Transanal Surgery: A History of taTME Ancestry

Abstract

Transanal total mesorectal excision (taTME) is the culmination of major developments in rectal cancer management and minimally invasive surgery. This surgical breakthrough holds great promise and excitement for the care of the rectal cancer patient. We would be remiss in discussing taTME to not acknowledge the role of transanal abdominal transanal proctosigmoidectomy, transanal endoluminal microsurgery, laparoscopy, and natural orifice transluminal endoscopic surgery that got us to this modern day explosion of the taTME approach. In this article, we detail and explain the convergence of these disparate experiences, how they culminated in the development of the taTME, and explore future directions in this field.

“We can see further because we stand on the shoulders of giants”

Sir Isaac Newton

Transanal total mesorectal excision (taTME) is the result of a variety of developments in both the understanding of rectal cancer as well as the surgical tools and techniques utilized in the operative care of the rectal cancer patient. For the majority of the 20th century, the abdominal approach to treating rectal cancer has varied little from the abdominoperineal resection (APR) Dr. Miles described in 1908. ¹ Starting in the mid 1980s and developing over the next 40 years, a variety of disparately linked events have come to shape the modern day treatment of rectal cancer and give birth to the taTME movement. In the 1970s to 1980s with local recurrence rates ranging from 20 to 40% and APR rates as high as 70 to 80% for the treatment of rectal cancer, clearly there was much room for improvement. ² From different points around the globe, contributions were made to form modern day care for the rectal cancer patient. Dr. Richard J. “Bill” Heald heightened the focus on the primacy of proper surgical technique in the treatment of rectal cancer, coining the term total mesorectal excision (TME). ^{3 4} TME has since become a cornerstone of rectal cancer surgery. Drs. Gerald Marks and Mohamad Mohuiddin in Philadelphia championed the notion of preoperative radiation therapy to downstage rectal cancer and extend sphincter preservation. This effort was furthered by Dr. Gerald Marks who described the transanal abdominal transanal (TATA) proctosigmoidectomy with descending coloanal anastomosis in 1984 to spare the sphincter, avoiding a permanent colostomy, for cancers of the distal third of the rectum, introducing the first experience of intersphincteric resection (ISR). ⁵ In 1983, in Tubingen, Germany, Dr. Gerhard Buess invented the transanal endoscopic microsurgical (TEM) platform. ^{6 7} He developed this for clear vision and reach within the confines of the rectum to resect en bloc rectal polyps and early cancers. In aggregate, these three events created the environment for the taTME approach to evolve.

The years between the late 1980s and 2010 introduced the forces that converged as a minimally invasive surgical (MIS) revolution. The laparoscopic era began with the presentation in 1989 at the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES) by Drs. Perissat and Mouiel of the first laparoscopic cholecystectomy. ^{8 9} This procedure resulted in a wildfire of laparoscopic approaches as the laparoscopic cholecystectomy quickly became the gold standard in the treatment of cholecystitis. Drs. Fowler and Jacobs, separately, reported performing the first laparoscopic colectomies in November of 1990. ^{10 11} The laparoscopic approach was then adopted by a variety of other fields and from there, the sky became the limit.

From this beginning a series of techniques have been developed with the goal of minimizing the surgical trauma of entry into the abdominal cavity. Single port colon surgery was developed by Curcillo in 2007 ¹² and was first performed and reported by Drs. Geisler and Remzi at the Cleveland Clinic later in 2007. ¹³ Separate from this but also in 2003, Drs. Rao and Reddy had begun to perform natural orifice transluminal endoscopic surgery (NOTES) using flexible endoscopes through the stomach to perform appendectomies in India. ¹⁴ Transanal minimally invasive surgery (TAMIS) was introduced by Drs. Albert, Larach, and Atallah to develop a low-cost approach for resection of rectal polyps. This approach proved to be better suited for more radical surgery being performed via transanal mode than the more rigid TEM platform. ¹⁵ While many of these advances were met with limited adoption, their aggregate is what gave birth to the taTME movement. It would be remiss in discussing taTME to not acknowledge the role of TATA, TEM, laparoscopy, and NOTES that got us to this modern day explosion of the taTME approach. In this article, we detail and explain the convergence of these disparate experiences and how they have culminated in the development of the taTME and explore the future directions of this field.

Challenges of Rectal Cancer Surgery

The real genesis of the taTME approach lies in the simple well understood fact that rectal cancer surgery is very difficult. The challenges of removing the cancer with negative margins, sparing the nerves and anal sphincter, and then being able to anastomose a neorectum to the low rectum or anus while working in the deep narrow pelvis has challenged surgeons dating back to the early 1900s. The central issues surround a series of questions: What constitutes a reasonable distal and circumferential margin? How is this obtained, particularly after the downstaging occurs after neoadjuvant therapy? How can one best accomplish this with the TME resection method highlighted by Heald? It is because of these challenges there has been such heightened attention to laparoscopic rectal cancer surgery, robotic TME, and now transanal TME to address these issues. Because of concerns regarding oncologic outcomes when applying the laparoscopic technique to colorectal cancer, initial adoption of laparoscopic surgery for colon cancer was quite slow and really did not pick up pace until the publication of the COST trial 15 years after the first laparoscopic colectomy was performed. ¹⁶ The same issues existed, causing even more reticence, addressing the much more technically challenging TME operation in a laparoscopic fashion for the treatment of rectal cancer. While laparoscopy raised theoretical concerns of pneumoperitoneum disseminating cancer cells and leading to carcinomatosis for colon cancer, for rectal cancer real practical technical issues existed. How would surgeons create three-dimensional (3D) retraction in the deep pelvis laparoscopically? How would an Endo GIA stapler be applied from above? What was the safety of multiple GIA firings across the rectal stump? With the loss of any tactile feel, how did the surgeon know, in applying a stapler from above, that an adequate distal margin had been obtained before applying the stapler to the rectum laparoscopically? In aggregate, these questions and issues simultaneously slowed MIS adoption for the treatment of rectal cancer and set the stage for the development of taTME.

In the world of minimally invasive surgery, two distinctive yet interrelated approaches were developing, both with the goals of minimizing the trauma of access to perform adequate surgery. Single incision laparoscopic surgery (SILS) was developed by Dr. Curcillo in 2007 ¹² and first performed for a colectomy by Dr. Geisler and Remzi at the Cleveland Clinic later in 2007. ¹³ The goal of SILS was to recreate the laparoscopic procedures while using a single incision to obtain superior cosmesis and less trauma of entry. In an effort to accomplish the same goals with a radically different approach, Drs. Rao and Reddy were performing transluminal resections of the gallbladder and appendix in India and introduced the concept of doing full-scale operations through the lumen of the bowel. ¹⁴ With the introduction of these techniques, there was a tremendous influx of interest both in the surgical community and in our industry counterparts. New instruments and methods of access became available to surgeons and they were applied with varying results. While the enthusiasm was great, many at the time questioned the intelligence of the NOTES approach. In 2009, Dr. John Marks presented at Digestive Disease Week and later published his opinions regarding this approach, raising the question of the wisdom of causing injury in a healthy organ to remove a diseased organ. ¹⁷ Additionally, the questions raised of intra-abdominal infection and carcinomatosis in the setting of a cancer were raised. However, in the colorectal field, this approach seemed more reasonable. With the rectum being both the access and target organ, the question was raised as to whether a NOTES-style approach could be applied with good benefit to the patient.

Coming from a totally different direction, TEM surgery had been going on for the past two decades. Originally, TEM teaching came with the warning that anterior lesions higher in the rectum could not be approached with TEM because of concerns regarding entry into the peritoneum. However, as surgeons became more experienced with TEM, indications and applications expanded. Drs. Winde and Buess had demonstrated the benefit of TEM surgery for improving margins and en bloc resections, avoiding fragmentation of the specimens due to the improved access and visualization in the lumen of the rectum. ^{7 18} Drs. Marks and Lezoche had applied TEM to full-thickness excisions of the rectal wall in the irradiated rectum for the treatment of select rectal cancers with great success. ^{19 20} While originally there had been great fear in entering the abdominal cavity because of concerns of carcinomatosis and pelvic sepsis, a growing body of literature supported the ability to do this in properly trained hands. In 2014, Marks' group published on the safety of entering the peritoneal cavity and performing a primary closure. ²¹ Larger excisions, even sleeve excisions with full preservation of the abdominal cavity, began to be performed. Through the experiences during this time period, the seeds of innovation had been sown, laying a foundation that would later allow for the expansion of this approach to more radical surgery.

Transanal Abdominal Transanal

The ancestor of the taTME approach developed entirely separate from these events and dates back to 1984 with the development of the ISR named the TATA procedure. Dr. Gerald Marks at Thomas Jefferson University developed this approach. ⁵ The two dominant drivers for this operation were to avoid a permanent colostomy in patients with cancers of the distal third of the rectum and to have a known distal margin after neoadjuvant therapy. However, it was also immediately well recognized, but not emphasized in publications, that by beginning the operation transanally, the most difficult portion was performed at the start of the operation. Compared with the standard of the day, a standard that exists to this day, in which these operations are approached from above with a challenging reach down into the deep pelvis, particularly in men, starting the operation immediately adjacent to the tumor, when the operative team was fresh and things could be clearly seen, offered an enormous benefit. In a time period where local failure rates were commonly in the 20 to 40% range, ² Marks and Mohuiddin were able to provide sphincter preservation for patients who would otherwise uniformly have a permanent colostomy and dropped local recurrence rates to 9%. ²² The hallmark of this approach is starting the dissection in a full-thickness fashion at the level of the dentate line, and continuing the incision through the full-thickness of the internal sphincter into the intersphincteric plane as an ISR. The rectum is oversewn and the dissection is taken cephalad, in the same avascular plane so well described by Dr. Heald, through the “angel hairs” up to the level of the seminal vesicles in men or the cervix in women.

It was in this background that more experimental work began. In 2007, Dr. Mark Whiteford, from Dr. Lee Swanson's group, performed the first cadaveric proctosigmoidectomy experience performed in a NOTES fashion. ²³ Drawing from their extensive experience with TEM surgery, and active involvement in the NOTES movement, Whiteford used a TEM platform to complete a TME transanally. This demonstrated, on a theoretical basis, how this could be performed.

Dr. Patricia Sylla, working under the direction of Dr. David Rattner, another strong proponent and pioneer of NOTES, worked to refine this technique by performing NOTES proctectomy in a series of cadavers. ²⁴ In collaboration with Dr. Antonio Lacy, she developed a systematic cadaveric approach to transanally initiated TME surgery. Dr. Lacy brought to the table a strong laparoscopic experience being a world leader to laparoscopic TME surgery and a major contributor to the COLOR II trial. ²⁵ He, however, recognized the inherent challenges in performing TME surgery laparoscopically and sought to collaborate to see if treatment of the rectal cancer patient could improve by applying a different MIS approach. Dr. Jung Ji Kim in Korea, who's mentor had trained with Dr. Gerald Marks at Jefferson, was also moving in a similar direction applying the TATA laparoscopically with similar outcomes, which he termed the laparoscopic abdominal transanal proctosigmoidectomy. ²⁶ These early cadaveric and clinical experiences demonstrated that the NOTES approach could greatly facilitate the challenges of laparoscopic retraction and visualization in rectal cancer surgery.

Modern taTME Era

The convergence of all of these techniques occurred in December 2008, when the first transanal TME was performed by Dr. John Marks in Philadelphia. Faced with a patient with metastatic rectal cancer, a laparoscopic Hartmann's procedure was planned. As this was performed, the dissection became very difficult and ultimately became impossible from above in a laparoscopic fashion because of tumor adherence to the right pelvic sidewall. Dr. Marks, who already had a large experience with laparoscopic TATA and the initiation of the rectal dissection from below, as well as TEM surgery, decided to attempt to apply these two techniques together to avoid an open conversion in this patient. The TATA was initiated transanally, the rectum was oversewn, and the TEM equipment was inserted. The dissection was carried cephalad from below, outside of the tumor plane laterally and subsequently the TME was completed from above. Ultimately, the specimen was removed transanally. While successfully performed, this was not published at that time. During this same period of time, Drs. Albert, Larach, and Atallah performed and described the TAMIS approach using a flexible single-port platform to perform endoluminal polypectomies in lieu of a TEM scope. ^{15 27} This was really a critical development in the birth of the taTME movement. The flexibility and further application of this format ushered in the taTME era. While some still use a rigid format for their taTME dissection, the ease and applicability of the TAMIS approach has expanded the horizons of taTME exponentially. Dr. Marks applied the TAMIS approach to radical resection in June of 2009 when faced with the task of removing residual rectum in a Crohn's patient with history of a total abdominal colectomy who had developed a rectovaginal fistula. Once the transanal dissection of the TATA had been performed and the rectum oversewn, the TEM scope was inserted and quickly identified as inadequate. Faced with the inflexibility of the TEM system and the challenge of needing to operate in the anterior 180 degrees, the SILS port was placed to complete the proctectomy, in a TAMIS. This was done with only a laparoscopic 5-mm port guidance from above, to allow a camera for guidance. It was in short order following this that Drs. Lacy, Rattner, Delgado, and Sylla performed their first NOTES transanal rectal cancer resection using TEM and laparoscopic assistance in 2009. ²⁸ Following this, Dr. Lacy, in conjunction with Drs. Rattner and Sylla, began a systematic, institutional review board-approved study of the transanal bottoms-up TME approach. ²⁹ They are to be credited with popularizing this approach, coining the term taTME and routinely applying laparoscopic techniques to the transanal portion of the TME in the TATA fashion.

Since its inception, a tremendous amount of work and intellectual activity has gone into the development of taTME. The initial questions, which still have not been definitively answered to the satisfaction of the widespread surgical community, surround the ability to properly perform a TME resection, the avoidance of carcinomatosis, and the ability to avoid intra-abdominal pelvic sepsis, having cut across the bowel giving access to the peritoneum of the pelvis and abdomen. To address concerns about TME quality, several publications exist. Marks et al performed a case-matched study comparing taTME and multiport laparoscopic TME, with 100 and 94.1% respective rates of complete or near-complete TME. ³⁰ de Lacy et al reported on the high TME quality with this approach in their experience with 186 patients with mid and low rectal cancers. ³¹ TME was complete or near-complete in 97.3%. Dr. Lacy's group also reported circumferential and distal margin positivity (≤ 1 mm) in 8.1 and 3.2% of patients, respectively. Denost et al showed in a randomized controlled trial that transanal approaches to TME are associated with reduced risk of positive circumferential margin compared with transabdominal TME. ³² Addressing concern for intra-abdominal pelvic sepsis with this approach, Dr. Lacy's group prospectively followed 140 patients showing that only 2.9% developed an intra-abdominal fluid collection. The anastomotic leak rate in this series was 8.6%, comparable to that reported in laparoscopic TME series. ³³

The more central and important questions in the care of the rectal cancer patient center around the oncologic efficacy of this approach and long-term outcomes with local recurrence rates, rates of distant metastases, the possibility of new unexpected metastatic scenarios, and long-term survival. Short-term outcomes reported by Dr. Lacy's group are encouraging. After a median of 15.1 months of follow-up in 140 patients, they report a local recurrence rate of 0.8%, systemic recurrence in 6.1%, and both local and systemic recurrence in 1.5%. ³³ Marks et al reported very promising long-term oncologic outcomes in their experience with TATA/taTME. ³⁴ In 373 patients, with mean follow-up of 5.5 years, local recurrence was 7.4%, distant metastasis was 19.5%, and Kaplan–Meier 5-year actuarial survival was 90% in a cohort in which 91% had cancer of the distal rectum and 76% presented with T3 tumors.

Additional energies have been centered on how to optimize the operative technique, standardize the approach, and apply safe training for surgeons to learn and practice this for their patients. As outlined by McLemore et al at the 2014 SAGES meeting, there are key elements in a successful training pathway. These include: expertise in TME for rectal cancer, expertise in MIS (both laparoscopic and robotic) TME from the abdominal approach, expertise in TEM, and experience in intersphincteric dissection. ³⁵ It is fitting that the modern rectal cancer surgeon should demonstrate mastery in each of the surgical techniques and skills that converged to become the modern taTME. Training courses with human cadaver laboratories such as Dr. Lacy's taTME course through the Advances in Surgery Channel in Spain and Dr. H.J. Bonjer's course in the Netherlands will be instrumental in wider adoption of taTME. In the U.S., Drs. Albert and Attalah in Orlando, Florida, have led the charge, having done significant work in the standardization and teaching of the taTME technique with thorough technical descriptions and cadaver laboratories. Their program trains 12 to 15 surgeons at a time and they have already trained hundreds of surgeons in this technique. ^{36 37} The iLappSurgery Foundation has provided an easily accessible application that increases access to taTME educational materials for all colorectal surgeons. ³⁸ Lastly, formal studies looking at training courses and their effectiveness have been adopted and are underway. ³⁹

The natural extension of the taTME movement has been to perform the entirety of the operation transanally. In France, Dr. Leroy first developed and performed the first “pure” NOTES proctosigmoidectomy with transanal completion of the TME dissection, liberation of the splenic flexure, transection of the inferior mesenteric artery (IMA) and inferior mesenteric vein, and coloanal anastomosis. He coined the procedure Perirectal Oncologic Gateway to Retroperitoneal Endoscopic Single-Site Surgery (PROGRESSS). ⁴⁰ Zhang et al successfully performed NOTES proctosigmoidectomy with taTME in Asia. ⁴¹ In Europe, Chouillard et al attempted 16 entirely transanal NOTES proctosigmoidectomy procedures and were able to complete the procedure with no abdominal incisions in 10 cases. ⁴² In the United States, Dr. John Marks published his own experience with pure NOTES proctosigmoidectomy with an emphasis on video demonstration of critical views for the operation including high ligation of the IMA and splenic flexure release. ⁴³ The limiting factor of pure NOTES is its extreme technical demand. As surgical technology and equipment continue to improve, the performance of more radical colorectal excisions by pure NOTES will undoubtedly increase.

Conclusion

The continued evolution and adoption of taTME will be an exciting chapter in the care of rectal cancer patients. The logic of starting the operation transanally, assuring a known distal margin and addressing the most difficult part of the operation first, is inherently obvious. While first recognized in the 1980s with the development of the TATA, it has evolved in the last three decades to its current practice with great potential benefit to rectal cancer patients. As new technology in the form of improved optics, 3D and 4K resolution, and single-port robotic platforms become more widely available, the ability of surgeons to carry out these operations for their patients will increase. Clearly, these developments will allow taTME to become more widely practiced. Of course, all of this will need to be challenged and tested vigorously. Formal studies are currently underway. The Multicenter Phase II Study of Transanal Total Mesorectal Excision (taTME) With Laparoscopic Assistance for Rectal Cancer, led by Dr. Patricia Sylla, is underway in the United States with 11 participating centers. The International taTME Registry that Dr. Hompes has organized has already gathered data on over 1,000 cases and has been used to show acceptable short-term patient outcomes with data from 23 countries. ⁴⁴ With this information, we should be in a better position to definitively state what the real benefits and risks are of taTME. It will be the responsibility of the current experienced minimally invasive rectal cancer specialists as well as young investigators to define the limits and ideal application of the bottoms-up approach. This significant step forward for our patients should be an exciting development to participate in and witness for all those involved.