Natural-orifice transluminal endoscopic surgery.

Review

Natural-orifice transluminal endoscopic surgery S. Atallah1 , B. Martin-Perez1 , D. Keller3 , J. Burke4 and L. Hunter2 1 Department of Colon and Rectal Surgery, Florida Hospital, and 2 University of Central Florida, Orlando, Florida, and 3 Colorectal Surgical Associates, Houston, Texas, USA, and 4 Centre for Colorectal Disease, St Vincent’s University Hospital, Dublin, Ireland Correspondence to: Dr S. Atallah, Department of Colon and Rectal Surgery, Florida Hospital, 242 Loch Lomond Drive, Winter Park, Florida 32792, USA (e-mail: [email protected])

Background: Natural-orifice transluminal endoscopic surgery (NOTES) represents one of the most

significant innovations in surgery to emerge since the advent of laparoscopy. A decade of progress with this approach has now been catalogued, and yet its clinical application remains controversial. Methods: A PubMed search was carried out for articles describing NOTES in both the preclinical and the clinical setting. Public perceptions and expert opinion regarding NOTES in the published literature were analysed carefully. Results: Two hundred relevant articles on NOTES were studied and the outcomes reviewed. A division between direct- and indirect-target NOTES was established. The areas with the most promising clinical application included direct-target NOTES, such as transanal total mesorectal excision and peroral endoscopic myotomy. The clinical experience with distant-target NOTES, such as for appendicectomy and cholecystectomy, showed feasibility; however, NOTES-specific morbidity was introduced and this represents an important limitation. Conclusion: NOTES experimentation in the preclinical setting has increased substantially. There has also been a significant increase in the application of NOTES in humans in the past decade. Enthusiasm for NOTES should be tempered by the risk of incurring NOTES-specific morbidity. Surgeons should carefully consider patient preferences regarding this new minimally invasive option, as opinions are not unanimously supportive of NOTES. As technical limitations are overcome, the clinical application of NOTES is predicted to increase. It is paramount that, when this complex technique is performed on humans, it is applied judiciously by appropriately trained experts with outcomes recorded in a registry. Paper accepted 20 October 2014 Published online in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.9710

Historical perspectives

The journey to natural-orifice transluminal endoscopic surgery (NOTES) began long before the endoscope was invented. A natural-orifice speculum for the purpose of diagnosis, and later surgery, has been in use since the Babylonian era (500 AD) when the vaginal speculum was described1 – 3 . The original natural-orifice transluminal surgery was, in fact, vaginal hysterectomy4 . This may have been performed as early as 50 BC by Themison of Athens5 , although the first authenticated vaginal hysterectomy was done by Berengario da Carpi of Bologna in 15076 . Mikulicz7 described transperineal rectosigmoidectomy in 1889, later popularized by Miles8 and Altemeier9,10 . Both of these procedures (vaginal hysterectomy and transperineal rectosigmoidectomy) have all of the fundamental elements of NOTES, except they were not endoscopic. In the early 1800s an open-tube system was devised with visualization achieved by kerosene lamp light and © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

mirrors. In 1865, Desormeaux presented the first rigid endoscope for cystoscopy and, with limited success, visualized the stomach2,3 . Rigid tubes evolved into rigid telescopic instruments, and an overheated electrically plated platinum wire was used as a light source until Edison invented the incandescent light bulb in 1880. Semiflexible instruments (whereby the distal tip of the scope could be angled 30∘ ) were developed by Johann Von Mickulicz in 1881. As early as 1898, the first flexible ‘gastrocamera’ was developed3 , which would later become modernized with the advent of fibreoptics and video cameras. The first fibreoptic endoscopy was performed in 1957, heralding the era of present-day endoscopy1 .

The modern NOTES era

The modern era of NOTES has been led principally by gastroenterologists. As gastrointestinal (GI) endoscopists BJS 2015; 102: e73–e92

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gained confidence and experience with their skill set, and as the field of interventional endoscopy expanded, they began pushing the limit of what could be accomplished endoluminally, eventually exiting the confines of the GI lumen entirely to perform surgery. The prequel to current NOTES, then, began with simple transluminal procedures that did not require pneumoperitoneum. In 1980, ‘gastrostomy without laparotomy’ was described for the first time in 12 children and 19 adults, representing a procedure that, with strict interpretation, met all the criteria of NOTES11 . Next, Khawaja and Goldman12 demonstrated that transluminal endoscopic drainage of a pancreatic pseudocyst was feasible, and this approach has been shown to be as effective as surgery13,14 . By the late 1980s, laparoscopy would become introduced to general surgery and would rapidly become the standard for many operations, especially cholecystectomy and appendicectomy15 . It was not only GI endoscopists who were further exploring and exploiting natural orifices as a means of access, it was also surgeons. In 1949, Bueno16 described a series of transvaginal appendicectomies performed without endoscopic assistance at the time of vaginal hysterectomy. Daniel Tsin also performed NOTES before its widespread introduction, using the transvaginal approach. This included transvaginal oophorectomy in 2002 and transvaginal cholecystecomy in 2003, although the latter was performed with laparoscopic assistance17 – 19 . Although remarkable, these human NOTES operations went essentially unnoticed by surgical communities. In 2004, Kalloo and colleagues20 performed the first transgastric periteonscopy in a porcine model. Next, Rao and Reddy21 demonstrated the first human transgastric NOTES appendicectomy. Although this milestone operation was oddly never published, it underscored the power of this entirely new category of minimally invasive surgery. Soon afterwards, the term NOTES was coined to describe this novel approach. In October 2005, a scientific working group was also founded and named Natural Orifice Surgery Consortium for Assessment and Research (NOSCAR) to study the safety, efficacy and indications, as well as the ethical use of NOTES in humans22,23 ; 5-year progress on NOTES was published subsequently24 . Extensive investigation was carried out in animal models and cadavers exploring the safety and efficacy of NOTES, with a gradual transition to phase I clinical trials25 – 28 . Soon another milestone was realized, with the first transgastric cholecystectomy in a human performed by Jacques Marescaux29 . Ten years later, NOTES represents one of the most intense areas of surgical and GI research, and is arguably the most significant surgical innovation since the advent of laparoscopy. © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

S. Atallah, B. Martin-Perez, D. Keller, J. Burke and L. Hunter

Working groups

Multidisciplinary working groups have been formed worldwide to provide direction for NOTES to study and report on outcomes. The Society of American Gastrointestinal and Endoscopic Surgeons (SAGES) and the American Society of Gastrointestinal Endoscopy (ASGE) joined to form NOSCAR in 200521 . In early 2007, the European Association for Endoscopic Surgery (EAES) and the European Society of Gastrointestinal Endoscopy (ESGE) joined to form the Euro-NOTES Foundation30,31 . In 2008, several initiatives on a national level were created, such as the working groups in Germany known as Deustchland-NOTES, or D-NOTES32,33 . Other societies such as the Australasian Society were also concerned about the safety and effectiveness of this novel technique, for which they reviewed the published literature and ongoing trials34 . Ensuring the judicious application of NOTES in clinical practice is one of the main objectives of these various working groups. Other objectives include driving the development of adequate instrumentation to overcome the technical limitations of NOTES procedures. Unlike most surgical society meetings, there is a strong emphasis on industry and new technology where surgeons, GI endoscopists and product design engineers can discuss solutions to existing challenges. Assessing yearly scientific progress and clinical outcomes is also an integral component for NOSCAR, Euro-NOTES and D-NOTES. Most of these committees hold yearly meetings, with expert-opinion guidelines or further implementation of NOTES based on existing data. Additionally, several national and international registries have been created in an effort to compile existing clinical data on NOTES procedures32 .

Division lines

When laparoscopy was introduced to general surgery in the late 1980s, it was heavily criticized as a ‘futureless technique’ and as ‘circus surgery … careless for the risk for patients’15 . Yet, less than a decade after its introduction, laparoscopy became standard, providing patients with a minimally invasive approach with proven benefit. However, unlike laparoscopy, the global adoption of NOTES remains nominal, and few possess the technical expertise to perform NOTES operations in clinical practice. The reasons for this are complex and multifactorial. Importantly, not all NOTES procedures are the same and there exist key division lines that separate the types of procedure performed. This imparts a different risk–benefit ratio for patients, and demands a different skill set for www.bjs.co.uk

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Table 1

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NOTES and its key subdivisions

Division

Examples

Type of operation performed Orifice used Distant-target versus direct-target organ Pure versus hybrid versus pure combined orifice

Cholecystectomy, appendicectomy

Flexible versus rigid instruments

Transoral, transvaginal, transanal Transanal TME (direct); transgastric appendicectomy (distant) Laparoscopically assisted pure transanal TME (hybrid); transvaginal appendicectomy (pure); transvaginal and transgastric nephrectomy (pure, combined) Transgastric appendicectomy (flexible gastroscopes); transanal TME (rigid, using TME or TAMIS)

NOTES, natural-orifice transluminal endoscopic surgery; TME, total mesorectal excision; TAMIS, transanal minimally invasive surgery.

surgeons/GI endoscopists. For example, a NOTES appendicectomy via a transgastric approach is not the same as a NOTES appendicectomy via a transvaginal approach. Therefore, it is hard to consolidate NOTES into one global entity, and the interpretation of outcome results in clinical trials can be confusing. It is important to recognize key differences that exist in different types of NOTES, as summarized in Table 1. They include: hybrid versus pure NOTES; division by type of orifice used to gain entry into the abdominal cavity; and, most importantly, division by whether or not direct-target versus distant-target NOTES is performed. Direct-target NOTES operations do not violate a healthy visceral organ to gain access to another, whereas a distant-target NOTES operation does. Examples of direct-target NOTES include peroral endoscopic myotomy (POEM), transanal total mesorectal excision (trans-TME) and vaginal-access minimally invasive surgery for NOTES hysterectomy (Fig. 1a,b)35 . Examples of distant-target NOTES include transgastric appendicectomy and transvaginal cholecystectomy. Distantand direct-target NOTES procedures are fundamentally different, and clinical application of direct-target NOTES, particularly with laparoscopic assistance, has increased exponentially in some fields, such as rectal cancer surgery, where trans-TME (fundamentally a NOTES operation with laparoscopic assistance) is performed increasingly by colorectal surgeons worldwide. Hybrid versus pure NOTES is another important division line. When laparoscopic incisions are used, there exists access trauma that could negate the advantages expected with pure NOTES. Thus, elimination of somatic pain is incomplete at best, and wound complications (principally infection and hernia) could still occur, while NOTES-specific morbidity is introduced. Furthermore, © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

a

Hysterectomy performed by vaginal-access NOTES

b

Experimental vaginal hysterectomy

a Vaginal-access minimally invasive surgery for hysterectomy represents a novel type of direct-target natural-orifice transluminal endoscopic surgery (NOTES). A multichannel access port, originally designed for transanal access, has been placed transvaginally. b In this cadaveric experiment, total vaginal hysterectomy was performed

Fig. 1

the advantages of decreased-access trauma are lessened with hybrid NOTES because the laparoscopic alternative is becoming less invasive36 . For example, laparoscopic port sizes have decreased from 12 mm, where fascia and skin are sutured closed, to 5 mm, where only skin closure is required, to 2⋅7 mm, where no closure at all is required. Furthermore, hybrid NOTES must also compete with other advanced laparoscopic techniques, such as multichannel single-port surgery which, when introduced through the umbilicus, is termed embryonic or E-NOTES by some authors37,38 . Most authors still view this as single-port surgery and not as a NOTES operation. Key challenges of NOTES today

There are ongoing challenges for NOTES. They include: a limited ability to establish spatial orientation; limited www.bjs.co.uk

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Table 2


Current limitations and challenges of NOTES

Spatial orientation Narrow working angles, distorted perspective Disorientation of the horizon Difficult to operate with retroflexion Insufflation Unregulated insufflations Establishing access Incision on a healthy organ (as for distant-target NOTES) 100 per cent enterotomy closure mandatory Seeding of bacteria and contamination of sterile cavity Instrumentation Difficult traction and countertraction Difficult management of bleeding Lack of feedback on force exerted on tissues Inability to triangulate Inability to use articulated instruments Inability to place additional ports if needed Need for combined hybrid techniques Availability of surgical theatre in case of conversion Skill set Need for previous laparoscopic and endoscopic skills Need for training for gastrointestinal endoscopists to work intra-abdominally

NOTES, natural-orifice transluminal endoscopic surgery.

ability to maintain a regulated and safe insufflation pressure while operating within the peritoneal cavity; complications of transvisceral access such as bacterial contamination of the peritoneal cavity; limitations of existing instrumentation; and lack of formal training programmes for surgeons and GI endoscopists (Table 2).

Spatial orientation and skill set Spatial orientation and familiarity with planes of view are critical in all modes of surgery. It has been well demonstrated that when vital structures are injured (such as the common bile duct during laparoscopic cholecystectomy) the most significant factor is not patient variant anatomy or severity of inflammation, but, rather, it is misperception caused by spatial disorientation39,40 . Because establishing spatial orientation with flexible scopes is difficult, and because lack of familiarity with the vantage points obtained may alter the perception of tissue planes, key structures could be injured inadvertently. Although this area of research is ongoing, endoscopic horizon stabilization for distant-target NOTES has not yet been developed41 , and NOTES experts must be able to operate flexible scopes in various configurations, including retroflexion; they must also be able to work inside the narrow scope axis. The scope axis is significantly narrower than the axis for single-port surgery, which is known to be a technically demanding platform. Thus, learning how © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

to perform NOTES procedures using a flexible endoscope, especially without laparoscopic assistance, requires advanced operator skill and the ability to adapt the limited spatial orientation. For NOTES procedures that use a flexible endoscope, it is difficult to gain proficiency because it requires prerequisite skill in both interventional endoscopy and laparoscopy.

Insufflation (non-hybrid intra-abdominal NOTES) Laparoscopy is typically performed with tightly regulated intra-abdominal pressure set to 15 mmHg, considered to be safe and effective at maintaining a stable pneumoperitoneum. Distant-target NOTES uses existing gastroscopes and other endoscopes that do not typically regulate and monitor pressure. If hybrid NOTES is performed, a standard laparoscopic insufflator can maintain stable pneumoperitoneum via a single trocar. If pure NOTES is performed, pressure regulation and monitoring are essential for safe intraperitoneal surgery. This represents an important modification that must be made to endoscopes if they are to be used for NOTES on humans. It has been shown that intra-abdominal pressure can be monitored, and thereby regulated, using pressure sensors, and when compared with sensors used for laparoscopy, the results correlate very closely42 . However, on-demand, unregulated endoscopist-controlled insufflators cause wide variations in intra-abdominal pressure, which can lead to potential haemodynamic compromise43,44 . In animal models, NOTES results in different haemodynamic changes from laparoscopy: a decrease in the diastolic blood pressure and widening of the pulse pressure are two effects on animals subjected to transgastric NOTES45 . In general, low (6 mmHg) on-demand endoscope pressure has been shown to be safer, and allows an acceptable operative view for transgastric peritoneoscopy46 . Other important physiological changes may be specific to NOTES, including a relatively increased incidence of thrombocytopenia47 .

Instrumentation Surgeons, endoscopists and the industry have worked to equip flexible scopes with the versatility needed to perform more advanced procedures. This also includes the ability to manage surgical bleeding quickly and effectively via the use of a novel nanopowder haemostatic agent (TC-325), which is able to control spurting arterial haemorrhage48 – 50 . This has already been approved for clinical use in Europe, but not in the USA. One of the major shortcomings of flexible instruments used for NOTES is that the devices themselves were never www.bjs.co.uk

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classified as robotic or mechanical59,60 . Mechanical systems include the EndoSAMURAI (Olympus Medical Systems), ANUBIScope™ (Karl-Storz, Tuttlingen, Germany) and dual-channel endoscope (Olympus Medical Systems). Robotic systems include the MASTER system (Nanyang University, Singapore), the ViaCath™ (Hansen Medical, Mountain View, California, USA)59 , as well as the TransPort® (USGI Medical, San Clemente, California, USA)61 . There has been increased interest in master–slave robotics for endoscopy and, although preliminary, they have proven application for submucosal dissection62 . These advancements are seen as a giant step forward towards forming a more powerful multitasking, flexible platform for both interventional endoscopy and NOTES63,64 . This area of research is ongoing, and a functional endoluminal mobile robot is in progress65 – 69 . Although ingenious, these miniature robotic platforms remain prototypes and have not yet been applied to humans. NOTES appendicectomy and cholecystectomy

The OverStitch™ (Apollo Endosurgery, Austin, Texas, USA) is shown here on the tip of a dual-channel Olympus scope. It allows the operator to automate suturing of viscera, particularly for closure of enterotomies. This is an example of how existing scopes can be retrofitted to meet the demands required for distant-target natural-orifice transluminal endoscopic surgery

Fig. 2

designed for advanced surgery. For the field to progress, the platform has to be remodelled so that it is able both to navigate the alimentary tract and to perform the necessary tasks of surgery51,52 . Modifications include steerable working channels and dual working arms that enable instrument triangulation51 . Closure of the enterotomy, necessary for transgastric distant-target NOTES, also requires device improvement. Innovations for NOTES closure using a flexible scope include the Eagle Claw (Olympus Medical Systems, Tokyo, Japan), OverStitch™ (Apollo Endosurgery, Austin, Texas, USA)52,53 (Fig. 2), over-the-scope-clip (OTSC) and T-bars. The efficacy of these devices is currently undergoing validation, and they are already in clinical use by advanced interventional GI endoscopists52 – 58 . New modalities for NOTES include more powerful flexible endoscopic, multitasking platforms, which can be © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

Laparoscopic surgery underwent an accelerated introduction into clinical practice, due mainly to the proven benefits of the laparoscopic cholecystectomy70 . In contrast, NOTES has yet to demonstrate advantages and a safety profile superseding that of traditional laparoscopy, without introducing NOTES-specific morbidity. The advocates of NOTES cite improved cosmesis71,72 , reduced systemic inflammatory response73 and the lack of postoperative pain29 as advantages. However, reduced postoperative pain has not been proven after NOTES cholecystectomy74 , and the marginal benefits in cosmesis must be balanced against the potentially increased morbidity. In clinical practice, distant-target NOTES with a flexible endoscope has been used primarily for elective cholecystectomy, with the transvaginal approach preferred over the transgastric approach. The second most common type of distant-target NOTES operation is appendicectomy. Tables 3 and 4 summarize clinical experience with these procedures30,75 – 95 . Table 5 summarizes important differences between transvaginal and transgastric NOTES access. Most NOTES appendicectomies and cholecystectomies use a hybrid, laparoscopically assisted technique96 . The outcomes in series describing more than 100 patients30,76,79,83,88,89,97,98 are listed in Table 6. The observed conversion rates of 0⋅9–11⋅2 per cent are higher than current standards for laparoscopic appendicectomy (1⋅0 per cent)99 and cholecystectomy (1⋅9 per cent)100 . These data reveal an overall complication rate of 1⋅4–14⋅7 per cent, which is higher than would www.bjs.co.uk

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Table 3


Clinical outcomes for NOTES appendicectomy

Reference

No. undergoing Age BMI Duration of Estimated Length of Conversion Postoperative Follow-up NOTES (years) (kg/m2 ) surgery (min) blood loss (ml) stay (days) rate (%) complications (%) (months)

Transgastric Rao et al.75 (2008) Zorron et al.76 (2010)* Kaehler et al.77 (2013) Transvaginal Palanivelu et al.78 (2008) Zorron et al.76 (2010)* Lehmann et al.79 (2010)*

10 14 15

n.r. n.r. 31⋅8

n.r. n.r. 26⋅3

n.r. 135⋅5 103

n.r. 25 n.r.

n.r. 3 3

20 n.r.† 7

10 21 13

n.r. n.r. 6

6 37 42

29⋅5 n.r. 36⋅5

n.r. n.r. 24⋅1

103⋅5 60⋅5 47⋅1

n.r. 26⋅4 n.r.

1⋅5 1⋅5 3⋅3

83 n.r.† 0

0 8 0

6 n.r. n.r.

*Articles reporting more than a single procedure; †rate of conversion not reported specifically by procedure except for transgastric cholecystectomy. NOTES, natural-orifice transluminal endoscopic surgery; BMI, body mass index; n.r., not reported. Table 4

Results of NOTES cholecystectomy procedures in studies of more than five patients

Reference Transgastric Asakuma et al.80 (2009)* Salinas et al.81 (2010)* Linke et al.82 (2010) Zorron et al.76 (2010)* Horgan et al.83 (2013)* Arezzo et al.30 (2013)* Transvaginal Zornig et al.84 (2008) Palanivelu et al.85 (2009) Asakuma et al.80 (2009)* Decarli et al.86 (2009) Pugliese et al.87 (2010) Salinas et al.81 (2010)* Zorron et al.76 (2010)* Linke et al.88 (2010) Lehmann et al.79 (2010)* Federlein et al.89 (2010) Cuadrado-Garcia et al.90 (2011) Hensel et al.91 (2011) Niu et al.92 (2011) Zornig et al.93 (2011) Noguera et al.94 (2012)* Horgan et al.83 (2013)* Arezzo et al.30 (2013)* Bulian et al.95 (2013)

No. undergoing Age BMI Duration of Estimated Length of Conversion Postoperative Follow-up NOTES (years) (kg/m2 ) surgery (min) blood loss (ml) stay (days) rate (%) complications (%) (weeks)

6 27 31 29 8 12

n.r. 46† 55 45⋅3† 41† 48⋅2

n.r. 30⋅5† 26 25⋅3† n.r. 24⋅8

138 137 n.r. 111 n.r. 125⋅4

n.r. n.r. n.r. 15⋅7 n.r. n.r.

2† 1 n.r. 1⋅5 1 2⋅4

0 n.r. n.r. 10‡ 0 0

0 18 0 24 0 0

n.r. n.r. n.r. n.r. n.r. n.r.

20 8 10 12 18 12 240 102 488 117 25 80 43 100 20 48 423 20

n.r. 34⋅5 n.r. n.r. 54 46† 45⋅3† 52⋅3 48⋅9 52⋅4 39⋅7 52 47⋅2 49 40⋅6 41† 42⋅6 44⋅8

< 40 27 n.r. n.r. n.r. 30⋅5† 25⋅3† 27⋅3 27 27⋅8 < 35 29 21⋅5 26 27⋅5 n.r. 26 28⋅1

62 148⋅5 116 125⋅8 75 147 96 n.r. 61⋅9 60⋅6 89⋅5 47 87⋅1 52 64⋅8 89⋅8 68⋅7 50

n.r. n.r. n.r. n.r. n.r. n.r. 12⋅4 n.r. n.r. n.r. n.r. n.r. 21⋅6 n.r. n.r. n.r. n.r. 0

2 4 2† n.r. 2⋅2 0 2 n.r. 3⋅2 2⋅8 1 3 2⋅7 2⋅1 1† 1 2⋅2 2

0 25 0 0 0 n.r. n.r.‡ 1⋅9 4⋅7 1⋅7 0 0 0 0 0 0 0⋅9 0

0 16 0 8 6 25 6⋅7 15 3⋅3 3⋅4 8 3 0 2 5 0 1⋅9 10

1 10 n.r. n.r. 48 n.r. n.r. 6 n.r. 4 24 12 26 5 64 4 n.r. 2

*Articles reporting more than a single procedure; †numbers refer to overall values rather than a single category; ‡rate of conversion not reported specifically by procedure except for transgastric cholecystectomy. NOTES, natural-orifice transluminal endoscopic surgery; BMI, body mass index; n.r., not reported.

be considered acceptable after appendicectomy (3⋅4 per cent) or cholecystectomy (4⋅8 per cent). Moreover, the high rate of major complications (up to 3⋅4 per cent) for these procedures requires emphasis. Most notable are NOTES-specific complications such as rectal wall injury89,97,79 , perforation of the urinary bladder30,79,98 , caecal injury requiring laparotomy30 , pelvic abscess formation after cholecystectomy30,79,97,98 , vaginal bleeding

and infection79,88 , gallbladder impaction in the proximal oesophagus during specimen retrieval, gastric fistula with peritonitis, oesophageal haematoma and oesophageal perforation76 . The safe, effective and judicious implementation of NOTES into clinical practice remains paramount. Currently, there is insufficient evidence to conclude that NOTES has a clear benefit over traditional laparoscopy or

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Important differences between transvaginal and transgastric NOTES

Transvaginal NOTES

Transgastric NOTES

Excludes half of the population Short distance to peritoneum; no other organs in transit

Can be applied universally Long distance to peritoneum requiring scope to navigate oesophagus and stomach before peritoneal entry 100 per cent closure is mandatory; closure requires multitasking platform or laparoscopic assistance Topical preparation is not feasible Only flexible instruments can be used to traverse stomach

Closure can be performed under direct vision and is not mandatory Vaginal mucosa can be prepared topically for sterilization Rigid (laparoscopic) or flexible instruments can be deployed transvaginally Orientation for cholecystectomy and appendicectomy is more similar to that for laparoscopy Concern by women about point of access, other than infection (e.g. dyspareunia, infertility) Vaginal specimen extraction carries low risk of adverse event

Spatial orientation and horizon stabilization for cholecystectomy and appendicectomy is complex No concern other than infection (e.g. 100 per cent closure) Oesophageal perforation during transoral specimen extraction has been reported in humans

NOTES, natural-orifice transluminal endoscopic surgery. Table 6

NOTES appendicectomy and cholecystectomy in clinical series describing over 100 patients Procedure

Reference

Enrolment

No. of patients

Arezzo et al.30 Federlein et al.89 Horgan et al.83 Lehmann et al.79 Linke et al.88 Mofid et al.98 Wood et al.97 Zorron et al.76

2007–2012 2007–2009 2007–2010 2008–2009 2008–2009 2007–2011 2008–2012 2007–2009

533 128 104 551 102 222 102 362

Appendicectomy

Cholecystectomy

Access

Converted (%)*

33 0 7 43 0 2 24 51

435 128 56 488 102 220 72 269

TV, TG TV TV, TG TV TV TV TV TV, TG

1⋅7 11⋅2 9⋅5 4⋅7 2⋅0 0⋅9 7⋅3 2⋅5

Overall complications (%)* 3⋅2 5⋅5 1⋅6 3⋅2 14⋅7 1⋅4 6⋅3 8⋅8

Major complications (%)* 2⋅1 3⋅1 0 1⋅7 2⋅0 1⋅4 2⋅1 3⋅4

*Rates for the index procedures of appendicectomy and cholecystectomy. NOTES, natural-orifice transluminal endoscopic surgery; TV, transvaginal; TG, transgastric.

other modes of surgery. Instead, the data reveal significant NOTES-specific morbidity, which should temper enthusiasm about this innovative approach. Peroral endoscopic myotomy

POEM arose in the context of NOTES as an incisionless, minimally invasive treatment for oesophageal achalasia101,102 . Endoscopic myotomy was first introduced by Ortega and co-workers103 for achalasia in 1980. The POEM technique was first tested in a porcine model, where Pasricha et al.104 described endoscopic myotomy through a submucosal tunnel. Perretta and colleagues105 then demonstrated the safety and feasibility in a porcine model. A key feature was the creation of a submucosal tunnel with closure of the mucosal entry site a distance away from the myotomy. Because of the mucosal incision and risk of perforation, this procedure was not initially accepted in humans104 . However, Inoue and co-workers106 – 108 elevated the endoscopic platform, developing POEM as a novel, safe and feasible technique for the treatment of © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

achalasia in humans. Since this initial work, the volume of POEM procedures performed worldwide has increased dramatically. Initial high success and low complications rates have driven the use of POEM, but its niche remains to be defined and long-term results are awaited109 . POEM has several benefits over traditional procedures for achalasia. It is similar to a surgical myotomy, but avoids abdominothoracic surgery, inherent external incisions, and associated postoperative care109 . Thus, patient recovery is expedited101,108,109 . The POEM procedure is especially beneficial for co-morbid patients with previous abdominal operations and morbid obesity, who would otherwise pose a significant operative risk. With POEM, there is greater surgical precision compared with surgical myotomy, as a selective circular myotomy is performed on the circular muscle layers of the lower oesophageal sphincter (LOS) affected by achalasia, preserving the anatomical integrity of the LOS110 . In addition, the operator can control myotomy length, and routinely perform a significantly longer myotomy106 – 108 . POEM also has a reduced risk of subsequent gastro-oesophageal reflux. In www.bjs.co.uk

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laparoscopic myotomy, mobilization of the oesophagus disrupts the angle of His and natural antireflux mechanisms, necessitating an antireflux procedure. In comparison, POEM leaves the hiatal attachments and angle of His untouched, so no antireflux procedure is necessary110 . Furthermore, improvement in symptoms is rapid; a recent study111 demonstrated that POEM can result in immediate correction of the non-relaxing LOS, promptly relieving dysphagia, heartburn and chest pain. Outcome studies to date have demonstrated that POEM provides definite relief of symptoms. Since 2008, Inoue’s group has performed POEM in more than 200 patients with symptomatic achalasia, with excellent short- and long-term results and absence of serious complications112 . In all patients, symptoms were ameliorated or greatly reduced. Resting LOS pressure was significantly lowered, and there were no procedural complications or deaths106 – 108 . During long-term follow-up, only two patients (1⋅0 per cent) required additional treatment: repeat POEM in one and pneumatic dilatation in another106 – 108 . Other centres have also reported their short- and long-term outcomes. Evaluating outcomes for 45 patients with achalasia in a single centre over 2 years, Chen and colleagues113 found that POEM significantly reduced the LOS resting pressure and symptoms of dysphagia, regurgitation, and chest pain after surgery. Ling et al.114 evaluated 87 POEM procedures after 5 days, and found significantly lower LOS pressure, reduced dysphagia, regurgitation and chest pain, improved oesophageal emptying and quality of life. They evaluated the patients again at least 1 year after POEM, finding that symptomatic relief and improvement in quality of life was durable114 . Sharata and co-workers115 followed 100 patients who had POEM over a 3-year interval at a single institution, and observed improved oesophageal emptying, and excellent relief of dysphagia (97 per cent) and chest pain (91⋅5 per cent). Although 38 per cent had residual reflux, more than half were asymptomatic and no patient required an additional antireflux procedure115 . Teitelbaum et al.116 also assessed 41 patients at a mean of 15 months after POEM, finding that 92 per cent achieved treatment success, with only 15 per cent reporting reflux symptoms. Zhou and co-workers117 followed 12 patients with persistent symptoms after Heller myotomy treated by POEM; after a mean 10 months of follow-up, 11 patients had treatment success, all had a lower mean LOS pressure, and only one had residual reflux symptoms. Thus, even after failed Heller myotomy, POEM is effective and results are durable. Although excellent results were reported from these single-centre series, a comprehensive POEM survey was created to evaluate the global experience118 . The International Per © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd


Oral Endoscopic Myotomy Survey (IPOEMS) involved 16 expert centres in three continents, evaluating a total of 841 POEM procedures. The survey found superior efficacy and safety outcomes in all centres, further supporting the transition to POEM for achalasia118 . POEM has changed the standard treatment for achalasia, and represents one of the most important applications of direct-target NOTES119 . The volume of POEMs performed worldwide has grown exponentially. Surgeons who performed Heller myotomy have embraced POEM as the preferred intervention for achalasia; the standard of care could possibly move from laparoscopic myotomy to POEM. However, the technique requires advanced endoscopic skills and a learning curve of at least 20 procedures120 . The low prevalence of achalasia, coupled with the advanced operator skill level required for the procedure, has limited the widespread integration of POEM. Formal training programmes are required to facilitate the implementation of POEM. Although long-term results are pending, POEM could become the treatment of choice for symptomatic achalasia111,121 . Transanal NOTES

Transanal NOTES is a fusion of four principal concepts and techniques, more than 30 years in gestation122 . In essence, it merges: transanal endoscopic microsurgery (TEM)123 /transanal minimally invasive surgery (TAMIS)124 ; the transanal–transabdominal operation (TATA)125 ; TME126 ; and, of course, NOTES. Gerald Marks pioneered the concept of the TATA operation for distal rectal cancer, particularly those within 3 cm of the anal verge, requiring en bloc resection. It was the prequel to transanal TME; there were advantages to TATA, including: identification of the distal margin first, to ensure an adequate (negative) margin; obviating the need for a double-stapled anastomotic technique, which had occasional technical problems due to the inability to access the distal bony pelvis, and perhaps inadvertent transection through, rather than distal to, the tumour; and increasing the likelihood of sphincter preservation for low-lying tumours while maintaining sound oncological principles125,127 . Meanwhile, the development of transanal NOTES was being pioneered, beginning with the initial work of Morris Franklin, who developed the technique of natural-orifice specimen extraction (NOSE) as an adjunct to laparoscopic sigmoid colectomy in 1993128 ; excellent long-term outcomes have been demonstrated, particularly with transanal as opposed to transvaginal NOSE129 . This technique has been further refined by Leroy and colleagues130 www.bjs.co.uk

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and Fuchs et al.131 . There are now multiple case series reporting the success of laparoscopic sigmoid colectomy and transanal extraction of the specimen (transanal NOSE)132 – 138 . In 2007, Whiteford, Denk and Swanström139,140 performed the first pure NOTES transanal rectosigmoidectomy using a TEM apparatus in a cadaveric model. Subsequently, Sylla, Lacy and co-workers141 performed the first NOTES transanal TME with laparoscopic assistance. As experience with this new approach increased using the new TAMIS platform, an important advantage to this type of NOTES was realized: it allowed excellent access for distal rectal and mesorectal dissection142 . The greatest value was realized when NOTES trans-TME was performed in men with visceral obesity143,144 . It maintains the advantages of direct-target NOTES, but also allows an in-line vantage point and improved access to the distal rectum122,145,146 . This changes the focus of the technique, which is no longer about minimizing access trauma, but rather about providing the best point of access for a given operation. Until the advent of trans-TME, distal rectal cancer in an obese man was a difficult challenge. This approach, however, solved the problem. Trans-TME is typically completed with a hybrid approach, although Zhang and colleagues147 , and subsequently Leroy et al.148 , have performed the first pure NOTES transanal TME in humans. More recently, Chouillard and co-workers149 reported the first small series of pure NOTES, with excellent outcomes. Table 7 summarizes clinical experience with trans-TME to date146,149 – 158 . The field of trans-TME continues to grow rapidly, with international adoption of the technique and continued modification, including adaptation of the da Vinci® Surgical System (Intuitive Surgical, Sunnyvale, California, USA) for robotic trans-TME159 – 162 (Figs 3 and 4). As with all new approaches, prerequisite skill and proficiency is necessary and hands-on training in trans-TME is crucial to ensure safe implementation of this NOTES technique. Although access to the distal rectum is excellent with trans-TME, there may be an increased risk of significant morbidity, such as urethral injury, owing to approaching the pelvis from a vantage point that most surgeons are not accustomed to using. In a series of 30 men undergoing trans-TME, there were two urethral injuries143 , a complication rarely encountered with traditional approaches to TME (including laparoscopic and robotic). This underscores the importance of appropriate training, and the need to enter NOTES trans-TME cases into registries whereby outcomes and surgical quality can be monitored163 . © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

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Transanal total mesorectal excision (trans-TME) is a new mode for performing rectal cancer surgery. This video still was taken during robotic trans-TME using the da Vinci® robotic surgical system (Intuitive Surgical, Sunnyvale, California, USA) and the GelPOINT® Path (transanal minimally invasive surgery) platform (Applied Medical, Rancho Santa Margarita, California, USA) for transanal access. Robotic transanal surgery is currently in development

Fig. 3

Fig. 4 The da Vinci® Sp (Intuitive Surgical, Sunnyvale, California, USA) is expected to be introduced into clinical practice in 2015. This single-arm, multichannel platform is predicted to have application for transanal total mesorectal excision, owing to its compact profile and flexible working instruments

Novel applications

Although laparoscopy was initially limited to simple procedures, the complexity and number of operations performed laparoscopically has grown substantially. Today, even the most complex procedures can be performed, such as laparoscopic pancreatoduodenectomy164 . Similarly, investigators have discovered novel applications www.bjs.co.uk

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Table 7


Transanal total mesorectal excision using NOTES Estimated blood loss (ml)

Length of stay (days)

Conversion rate (%)

Complications (%)

No. of LNs

Follow-up (months)

Platform

n*

Duration of surgery (min)

Zhou et (2006)

Transanal retractor

25

n.r.

n.r.

n.r.

n.r.

12

n.r.

70

Velthuis et al.151 (2013) de Lacy et al.152 (2013) Sylla et al.153 (2013) Marks et al.154 (2013) Atallah et al.146 (2013) Sourrouille et al.155 (2013)

TAMIS

5

175

n.r.

n.r.

0

40

12

n.r.

TAMIS

20

235

45

6⋅5

0

20

15⋅9

1

TEO

5

274

166

5⋅2

0

60

33

5⋅4

106

n.r.

476

n.r.

0

13⋅2

12

38⋅6

20

243

153

4⋅5

0

65

22⋅5

6

TAMIS

7

290

100

12

8

23

14

13⋅2

Wolthuis et al.156 (2014)

TAMIS

14

55‡

48⋅5

8⋅7

18

42

n.a.

6⋅3

Chouillard et al.149 (2014) Velthuis et al.157 (2014) Zorron et al.158 (2012)

TAMIS

16

265

225

10⋅4

6

19

21

9

TAMIS

25

n.r.

n.r.

n.r.

n.r.

n.r.

14

n.r.

TAMIS

9

311

95⋅6

7⋅5

11

22

13

n.r.

252

231

163⋅6

7⋅8

4⋅8

31⋅6

17⋅5

18⋅7

Reference al.150

Transanal retractor TAMIS

Mean†

Comments Overall survival 88%; longest follow-up 100% complete mesorectum 100% complete mesorectum

Largest series to date 90% complete mesorectum Conversion rate 7⋅7%; 85% complete mesorectum TAMIS proctectomy for benign procedures 10 cases of pure NOTES

Use of flexible endoscope transanally

*Number of patients in the study undergoing transanal total mesorectal excision; †except for total number of patients; ‡refers only to transanal resection. LN, lymph node; n.r., not reported; TAMIS, transanal minimally invasive surgery (using GelPOINT® Path; Applied Medical, Rancho Santa Margarita, California, USA); TEO, transanal endoscopic operation; n.a., not applicable.

for NOTES, and the spectrum of this growing field has broadened dramatically. For example, NOTES has been used successfully with the bladder as a point of access165 ; in animal model feasibility studies, it has been demonstrated that a NOTES transvesical approach can be used to perform peritoneoscopy166 and even thoracoscopy for lung biopsy167 . NOTES abdominal solid-organ surgery is also feasible, and both splenectomy and liver biopsy have been reported in animal models168 . Kantsevoy et al.169 have demonstrated the feasibility of splenectomy in a porcine model. However, once the spleen was resected, it was then delivered into the stomach without morselization and a retrieval mechanism was not achieved. This underscores the practical limit of what can be achieved with the pure NOTES approach. In addition to intraperitoneal surgery, it has been shown that NOTES can be applied to retroperitoneal structures170 . Upper-pole partial nephrectomy with transgastric access using thulium laser and laparoscopic (Veress needle) assistance for irrigation, smoke evacuation and

insufflation for a stable pneumoretroperitoneum has been reported by Boylu and colleagues171 , and Isariyawongse et al.172 have shown in a porcine model that a pure combined (transgastric and transvaginal) NOTES nephrectomy is feasible. Perretta and co-workers173 have shown that a transvaginal retroperitoneal NOTES adrenalectomy is feasible in a porcine model, and this has now been carried out successfully in humans174 . In some Asian cultures, aversion to neck incisions has led to alternative approaches to thyroidectomy175,176 , most notably transaxillary robotic thyroidectomy177 . Alternatively, Benhidjeb and colleagues178 demonstrated the feasibility of a totally transoral NOTES thyroidectomy in five cadavers. Although this new approach was done effectively in cadaveric series, human application would mandate proper identification of key anatomical structures, such as the laryngeal nerve. Furthermore, the healing process, including somatic pain from sutures of the oral mucosa after specimen extraction, has not yet been addressed179 .


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There have been other novel applications of NOTES, including both transgastric and transvaginal ventral hernia repair180 – 182 . A major concern with this approach, however, is bacterial contamination of prosthetic mesh183 . Transgastric small bowel resection in swine has also been described by Fuchs et al.184 , although this was completed with laparoscopic assistance. In aggregate, these innovative, novel applications of NOTES typify the interest of surgeons and interventional endoscopists. It also illustrates the broad scope and the potential for unique clinical applications for NOTES. Public perceptions

When a transition was made from open to laparoscopic surgery, the public was quickly convinced of the advantage, with the simple explanation that the same operation can be done with smaller incisions. But NOTES is different. Patient perceptions about violating one visceral organ en route to operating on another are more cautious. When the second White Paper on NOTES was written, summarizing 5 years of progress, the members of NOSCAR recognized that technical challenges could be overcome, but one block to further NOTES advancement was public preference24 . Multiple publications77,185 – 196 have addressed the question of patient perceptions about NOTES. Public support for NOTES is partial, and in most surveys preference for NOTES has yet to be realized. For example, in one study77 in which patients with early, uncomplicated appendicitis were offered a NOTES appendicectomy via a transgastric approach, only 15 of 111 patients opted for the procedure after it was properly explained. Hagen et al.197 surveyed 300 individuals, and their opinions on NOTES were obtained. Across all age groups, patients felt the cosmetic result was important, and were interested in scarless surgery. However, patients would accept only a 10 per cent increased operative risk in order to achieve a scarless cosmetic result. There are probably different perceptions about NOTES within society. Although it did not reach statistical significance, Lamadé and co-workers185 demonstrated that patients with poor body image (high negative body index) are more likely to accept an increased risk and spend additional money to undergo scarless or even scar-reduced (NOTES) abdominal surgery. Swanstrom and colleagues186 surveyed 192 patients (79 per cent of whom had a college education) to assess their perception of NOTES. NOTES was thought to require more skill than laparoscopic or open surgery and, interestingly, to pose less risk of complications than laparoscopy for the same procedure. Overall, a small majority (56 per cent) preferred NOTES as the method of choice for © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

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cholecystectomy. The authors concluded that, as long as the surgeon had the appropriate skill, NOTES was the favoured approach186 . Similarly, a study from China by Li et al.187 showed that laparoscopic surgery was preferred by 42⋅1 per cent of 1797 polled, and NOTES was preferred slightly more often (44⋅6 per cent). In yet another study by Rao and colleagues195 , NOTES was the least preferred method of surgery among 736 UK residents surveyed, with single-port and minimally invasive laparoscopy preferred by the majority, including the majority of the 251 male and female doctors in the study. In these studies, which are designed to understand public perceptions of NOTES, safety was the most important variable in choosing the type of surgical procedure preferred. This finding was echoed by Kim and co-workers188 : 84 per cent of 486 surveyed believed NOTES should be as safe as other surgical methods. Not surprisingly, safety of NOTES was the single most significant factor in most public opinion surveys across a broad socioeconomic spectrum189,190,196 . The specific concerns of women about transvaginal approaches for NOTES have been addressed by Peterson et al.191 . When 100 women (aged 18–79 years) were asked about transvaginal NOTES, more than 80 per cent had concerns about infection and dyspareunia. Cosmesis and scar reduction was important to only 39 per cent of women surveyed. The majority of women felt that hernia reduction (90 per cent) and decreased pain (93 per cent) were important advantages of transvaginal NOTES. Although women were interested in transvaginal NOTES, the majority did not recommend the procedure over other laparoscopic techniques; it is not accurate to conclude that women have a truly ‘positive’ perception of transvaginal NOTES192 . This was also demonstrated in another study by Strickland et al.193 , in which 78 per cent of 195 surveyed female healthcare workers did not favour NOTES transvaginal cholecystectomy over laparoscopic cholecystectomy, even if the two techniques were equally effective and safe. If NOTES transvaginal surgery was equally effective and posed the same surgical risk as a laparoscopic approach, Thele and colleagues194 reported that only 28⋅8 per cent of gynaecologists would recommend NOTES over standard laparoscopy. Indeed there are differences in basic factors, such as what defines risk (for example, severity and incidence of complications), that could influence how patients respond to surveys. For example, did the patients surveyed have a context as to what the predicted rate of hernia formation is after laparoscopic surgery? In fact, the risk of hernia after laparoscopy has been shown to be around 1 per cent198,199 . Because the public does not have the appropriate background in risks of surgery, and because they may www.bjs.co.uk

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not appreciate the difference between, for example, abdominal infection from gastric leak with NOTES access versus wound infection from laparoscopic access, interpreting the results of public surveys must be done cautiously. Furthermore, although the public perceives NOTES with enthusiasm, particularly when presented as a scarless alternative to laparoscopy, there remains anxiety about this new modality. Survey results are not uniform, but they point to a hesitation in the public’s recommendation of this new mode of surgery. These survey studies are important as they contribute to our understanding of medical anthropology and the biocultural adaptation of society to surgical innovation, which likely occurs gradually over time. Discussion

It has been a decade since Kalloo’s work catapulted surgeons and endoscopists into the modern NOTES era. The intrigue of scarless surgery and the quest to innovate surgical care has resulted in a headlong rush not unlike the internet dotcom frenzy of the 1990 s200 . To date, hundreds of publications have been written delineating new procedures, approaches, techniques and instrumentation, with the purpose of expanding the horizon of NOTES and improving its various and sundry platforms. A decade after the inception of NOTES, this realization has become quite evident: NOTES is no longer one generic type of surgery, and there exist deep division lines within this heterogeneous category of surgery. Perhaps the most important division line is between direct-target versus distant-target NOTES. Direct-target NOTES shows immediate promise for more widespread clinical application as the approach avoids the fundamental flaw of indirect, distant-target NOTES: purposely violating a normal, healthy organ to gain access to a distant, target organ. Perhaps the best examples of direct-target NOTES are POEM and trans-TME. The latter, which is typically performed as a hybrid NOTES operation, has received significant international attention and has been described as a technique that could revolutionize the approach to rectal cancer surgery142 . The key reason why hybrid NOTES trans-TME has become so promising is the excellent visualization of the distal one-third of the rectum and mesorectal envelope, which is particularly appreciated in men with a narrow pelvis and morbid obesity. Likewise, direct-target NOTES for POEM offers direct access to the surgical site, with excellent visualization to complete an otherwise invasive procedure. These advantages of direct-target NOTES have usurped the original quest for scarless surgery. Notwithstanding, there is a role for distant-target NOTES, particularly under special circumstances. © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd


Applications of distant-target NOTES could be fitting, particularly where the traditional approach is more hazardous. For example, in the first human transgastric appendicectomy described by Rao and Reddy21 , the patient had severe abdominal wall burns which made abdominal access less desirable. Other important examples include: patients who are too infirm to undergo general anaesthesia (such as critical care patients); superobesity; and abdominal wall hazards (such as thermal or chemical burns, connective tissue tumours, necrotizing fasciitis or contracture deformity). There may also exist relative indications for NOTES where, for cultural and social reasons, scar aversion exists, as exemplified by some Asian cultures178 . As for choice of orifice for abdominal access, there is currently a preference for vaginal over gastric access for distant-target intra-abdominal NOTES, because complications of vaginal wall closure are less significant than those of failed alimentary tract closure. Vaginal access may also be preferred because specimen extraction via this route is safe, and surgeons have already developed experience with this approach for specimen retrieval after gynaecological procedures. Obviously, the main disadvantage of transvaginal NOTES is that it is sex-specific. It should be noted that incursion through a healthy visceral organ, a prerequisite for distant-target NOTES, is not unique. In open abdominal surgery, there are several examples where healthy viscera are incised with the objective of gaining direct access to a target organ. Examples include incision of the anterior gastric wall to drain a pancreatic pseudocyst, incision of the bladder wall for ureteric reimplantation after psoas hitch, and enterotomy in the terminal ileum for extraction of gallstone ileus. They are not controversial, perhaps because surgeons believe that proper closure of a lumen can be assured by direct suturing. From a surgeon’s perspective, the durability of closure is fundamental to assure safety. Distant-target NOTES closures must therefore be as safe and reliable as surgical techniques. In the inaugural NOSCAR meeting in October 200522 , it was determined that 100 per cent gastric closure was necessary for distant-target transgastric NOTES, and this resolve remains unchanged today. In addition, the NOTES extraction process must be safe, particularly for transoral extraction of resected specimens that must traverse the narrow and relatively fragile oesophagus. For transoral gallbladder extraction during distant-target NOTES using a transgastric approach, no specimen entrapment or oesophageal perforation during specimen transit is permissible, yet both have been reported in clinical practice, representing examples of unacceptable, NOTES-specific morbidity76 . www.bjs.co.uk

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Interpreting the results of published data on NOTES remains arduous, not only because of the inherent heterogeneity, but also because publication bias is likely, with a tendency for investigators to report favourable results. NOTES registries may help establish more accurate outcome measures, but this requires all NOTES procedures to be recorded. There also remains a lack of adequately powered randomized clinical trials on NOTES, which limits the understanding of this new treatment modality with regard to efficacy, safety, benefit and cost, all of which guide evidence-based medical practice. Placed in context, the process of determining the benefit of laparoscopy over open surgery is still ongoing for some fields, such as rectal cancer surgery201 . In this sense, NOTES has yet to be explored to the same degree as other surgical innovations, including laparoscopy and robotic surgery. A razor-thin line separates innovation from experimentation. In future it is important that NOTES procedures are performed under institutional review board approval with the appropriate patient education, which should include informed consent that NOTES imposes surgical risks that are not inherent in traditional or laparoscopic surgery. It is also important that surgeons and GI endoscopists apply NOTES only when it is the optimal method for a patient. The final important question is who should be doing NOTES procedures and what training is required? In some settings the answer is clear. Trans-TME should be performed only by experienced rectal surgeons. Although not yet formalized, combined didactic and cadaveric training sessions in trans-TME are recommended for those who possess the appropriate skill set and experience. For other types of NOTES, particularly distant-target procedures that demand the use of a flexible endoscope, it is less clear who is qualified to perform operations such as NOTES transgastric cholecystecomy. Furthermore, a training programme has not been established. Currently, few surgeons and endoscopists have the facility to perform such complex procedures, or even basic NOTES procedures. For example, even a simple, iatrogenic enterotomy caused during routine colonoscopy is still managed by surgical referral and not by enterotomy closure using NOTES techniques. For some types of NOTES (in particular, distant-target NOTES), a team approach with GI endoscopist and minimal-access surgeon remains the safest method. Student training will be required, together with post-training experience, to master these complex techniques202 .

Disclosure

The authors declare no conflict of interest. © 2015 BJS Society Ltd Published by John Wiley & Sons Ltd

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BJS 2015; 102: e73–e92

Copyright of British Journal of Surgery is the property of John Wiley & Sons, Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.

Natural orifice transluminal endoscopic surgery for intra-abdominal emergency conditions.

Urological applications of natural orifice transluminal endoscopic surgery (NOTES).

Natural orifice transluminal endoscopic surgery and upper gastrointestinal tract.

NOViSE: a virtual natural orifice transluminal endoscopic surgery simulator.

Natural Orifice Transluminal Endoscopic Surgery: Reality or Myth?

Pure natural orifice transluminal endoscopic surgery (NOTES) involving peroral endoscopic salpingo-oophorectomy (POESY).

Shifting Paradigms in Minimally Invasive Surgery: Applications of Transanal Natural Orifice Transluminal Endoscopic Surgery in Colorectal Surgery.

Transtracheal thoracic natural orifice transluminal endoscopic surgery (NOTES) in a swine model.

Anesthetic management of transoral natural orifice transluminal endoscopic surgery: two cases report.

Comments on the current status and future development of natural orifice transluminal endoscopic surgery.

A miniaturized robotic platform for natural orifice transluminal endoscopic surgery: in vivo validation.

Robotic natural orifice transluminal endoscopic surgery (R-NOTES): literature review and prototype system.

The evolving practice of hybrid natural orifice transluminal endoscopic surgery (NOTES) for rectal cancer.

Thyroidectomy using pure natural orifice transluminal endoscopic surgery in a porcine model.

Hysterectomy by transvaginal natural orifice transluminal endoscopic surgery (NOTES): a series of 137 patients.

Endoscopic transluminal necrosectomy in necrotising pancreatitis: a systematic review.

Embryonic natural orifice transluminal endoscopic surgery in the treatment of severe acute pancreatitis complicated by abdominal compartment syndrome.

On the suitability of Thiel cadavers for natural orifice transluminal endoscopic surgery (NOTES): surgical training, feasibility studies, and anatomical education.

HALON-hysterectomy by transabdominal laparoscopy or natural orifice transluminal endoscopic surgery: a randomised controlled trial (study protocol).

Natural orifice transluminal endoscopic surgery-assisted versus single-port laparoscopic-assisted vaginal hysterectomy: a case-matched study.

Hybrid Natural Orifice Transluminal Endoscopic Surgery with Sentinel Lymph Node Navigation for Deep Early Gastric Cancer in the Fundic Region.

Natural orifice transluminal endoscopic surgery in humans: feasibility and safety of transgastric closure using the OTSC system.

Natural orifice transluminal endoscopic surgery-assisted versus laparoscopic ovarian cystectomy (NAOC vs. LOC): a case-matched study.

Role of transgastric natural orifice transluminal endoscopic surgery in the diagnosis of ascites of unknown origin (with videos).