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The art of bowel surgery in gynecologic cancer
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    1. 1 Gynecology and Obstetrics, Clinica Universidad de Navarra, Pamplona, Spain
    2. 2 Gynecology and Obstetrics, Clinica Universidad de Navarra, Madrid, Spain
    1. Correspondence to Dr Luis Chiva, Departamento de Ginecologia y Obstetricia, Clinica Universidad de Navarra, Pamplona, Spain; lchiva{at}unav.es

    Abstract

    The field of gynecologic oncology has witnessed a profound transformation in the practice of bowel resection over the years. This evolution, driven by innovative techniques and expanded surgical skills, has redefined the role of the surgeon. This review article delves into the historical journey of bowel surgery, its contemporary importance in cytoreductive procedures for gynecologic cancers, and the general principles of digestive surgery. From pioneering surgeons such as Lane, Broca, and Billroth to the introduction of mechanical staplers, this narrative unfolds the remarkable advances in the field. It highlights the critical need for meticulous training, anatomic mastery, aseptic measures, vascular support, tension-free anastomoses, and precise surgical techniques. These principles underpin the success of bowel resection and anastomosis in the complex landscape of gynecologic oncology.

    • Surgical Oncology
    • Ovarian Cancer

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    Background

    The practice of bowel resection in the field of gynecologic oncology has undergone a remarkable transformation over the years. This evolution has been marked not only by the development of innovative techniques but has also witnessed a significant expansion of the surgeon’s skill set.

    In this review, we will delve into the various aspects that constitute the art of bowel resection. To do so, we will study the historical trajectory of intestinal surgery. We will explore the current role of this surgery in cytoreductive procedures in gynecologic cancer. Finally, as the main objective of the article, we will describe the general principles of digestive surgery.

    Pioneering Steps: The Dawn of Intestinal Anastomosis

    The historical journey of intestinal surgery began with pioneering steps, and among the first surgeons to venture into this field were Sir William Arbuthnot Lane, Auguste Broca, and Theodor Billroth.1 Lane, a British surgeon, carried out pioneering work in intestinal anastomosis in the late 19th and early 20th centuries. He introduced the concept of end-to-end anastomosis,2 making significant contributions to the evolution of surgical techniques. In France, Auguste Broca, a contemporary of Lane, made notable contributions to this field. Theodor Billroth, a renowned Austrian surgeon, is known for his contributions to gastric surgery, which laid important foundations for surgical innovations in the abdomen, including intestinal resection (Figure 1).3

    Figure 1

    Professors Theodor Billroth and William Arbuthnot Lane.

    As for advances in suturing techniques, these were mainly driven by renowned figures such as Alexis Carrel and Charles Mayo.4 Alexis Carrel, a French surgeon, developed innovative techniques for vascular and intestinal anastomosis. His work with suture materials and fine needles laid the foundations for modern surgical practices. In the United States, Charles Mayo made significant contributions to surgical techniques, perfecting the art of suturing and anastomosis, especially in abdominal surgery.

    The 20th century witnessed a transformative change in intestinal surgery with the introduction of mechanical staplers, pioneered by surgeons like Michael DeBakey and John Ford.5 These surgeons played a crucial role in adapting and popularizing stapling devices for various surgical applications, including intestinal resection. Their contributions revolutionized the field, allowing contemporary surgeons to perform more precise and effective anastomoses.

    Current Role of Bowel Resection in Gynecologic Oncology

    The complex pelvis is a common scenario in gynecologic oncology in many situations, such as patients with peritoneal carcinomatosis, previously radiated or operated patients, tumor recurrences, as well as severe complications such as intestinal obstructions or anastomotic leaks.

    For years in gynecologic cancer, the “frozen pelvis” has been considered an unresectable disease, especially in countries without specific training programs. In the last three decades, we have witnessed incredible achievements in ovarian cancer surgery. Thanks to the pioneering work of Dr. Robert E. Bristow, complete cytoreduction has become the primary goal to achieve the best survival outcomes. Intestinal resection (whether colorectal or small intestine) is an indispensable maneuver to achieve complete cytoreduction.6 7 Similarly, total or posterior pelvic exenteration in primary or recurrent surgery will also require intestinal resection of one or more segments of the digestive tract, either in the exenterative phase or in the reconstructive surgery phase.8 9

    The rate of bowel resection in advanced ovarian cancer ranges from 25% to 50%, with colorectal resection being the most commonly performed procedure followed by an end-to-end colorectal anastomosis.10 11 Anastomotic leak remains the main concern after colorectal anastomosis, with a reported incidence of 1.26% to 9% in ovarian cancer patients.12–20 This complication correlates with heightened morbidity and mortality, prolonged hospital stays, and potential delays in administering chemotherapy.21

    Following colonic anastomosis, three potential approaches are considered: conservative management, a diverting ileostomy, or a ghost ileostomy. The ghost ileostomy, emerging as an alternative to a diverting ileostomy in ovarian cancer cases, offers distinct advantages.22 It can be readily converted into a diverting ileostomy if there are suspicions of anastomotic leak, thus minimizing the impact of fecal peritonitis. Moreover, in instances without anastomotic leak, it avoids the necessity for a stoma. Notably, unlike diverting ileostomy, reversal of the loop in patients without anastomotic leak can be achieved without re-laparotomy. This stands in contrast to diverting ileostomy, which mandates a subsequent surgical procedure for reversal. Importantly, the ghost ileostomy also mitigates the psychological and quality of life effects associated with a diverting ileostomy.23

    Hence, the ghost ileostomy presents itself as a viable alternative to diverting ileostomy, effectively circumventing its limitations and demonstrating advantages over routine diversion and a wait-and-see approach for ovarian cancer patients undergoing colorectal anastomosis.24 The ultimate decision regarding the necessity and type of diversion will hinge on the surgeon’s discretion as there is no definitive recommendation with respect to which patients would benefit from diverting ileostomy.25

    Regardless, the outcomes of these procedures are closely related to training and adherence to some crucial rules. In 2017, Chiva and colleagues published a survey highlighting the need for digestive surgery training among members of the European Society of Gynaecological Oncology.26 In the era of developing innovative adjuvant and maintenance therapies, ultra-radical surgeries are likely to become less frequent and, therefore, more demanding.

    General Principles of Bowel Resection and Anastomosis

    Nowadays, any gynecologic oncologist must be highly trained and skilled in mastering the field of digestive surgery and its potential complications. To achieve this, there are ten general principles that must be respected (Figures 2–4)27:

    1. Pre-operative and post-operative patient optimization: Ensuring adequate pre-operative nutrition and implementing pre-habilitation and Enhanced Recovery After Surgery (ERAS) programs will help reduce the risk of complications.28

    2. Master the surgical anatomy: A deep understanding of the surgical anatomy of the digestive tract is essential to successfully approach intestinal resection. Surgeons must be familiar with the anatomic architecture of each section of the digestive tract as well as its vascularization. The superior mesenteric artery and the inferior mesenteric artery are the two main vascular systems that supply the small and large intestine. Venous drainage is collected by the inferior mesenteric vein and superior mesenteric vein, which, along with the splenic vein, form the portal vein. Knowledge of the anatomic relationships of the different arterial branches and collateral mesenteric communications is crucial in the context of intestinal resection.29

    3. Maintaining asepsis and preventing the spread of intestinal contents: Measures should be implemented during bowel resection to prevent the spillage of intestinal contents by placing gauzes around the area to be resected and disposing of any materials that have come into contact with the intestinal lumen. Mechanical bowel preparation alone is not routinely recommended; however, if mechanical bowel preparation is performed, it should be combined with oral antibiotics to reduce post-operative complications.28

    4. Ensuring adequate blood supply: To ensure adequate vascular support for our anastomosis, there are two resources available. The first is to perform the anastomosis at the end of the cytoreduction procedure, allowing an assessment of the appearance and color of the intestinal stump. As an alternative trick, indocyanine green (ICG) can be used, especially in monochromatic settings, to check for intestinal ischemia.30 In any case, it is crucial that intestinal resection, whether small or large intestine, is performed while respecting vascularization. At a minimum, one arterial and one venous pedicle must always be preserved. Regarding colorectal resection, it is advisable to preserve the mesorectum whenever possible, to reduce the occurrence of the so-called low anterior resection syndrome (LARS).31

    5. Tension-free anastomosis: There are some resources to facilitate a tension-free anastomosis with a low risk of dehiscence and leakage. One of them is to perform the resection of the intestine in the healthiest segment closest to the tumor, whenever the tumor’s biology allows it. This will save intestinal resection length. Another even more important resource is to perform proper intestinal mobilization through retroperitoneal exposure maneuvers known as the Cattel–Braasch maneuver, Kocher maneuver, and Mattox maneuver.32 33 If this is not sufficient, the inferior mesenteric artery and/or vein can be ligated at their origins to gain distance and reduce tension. The superior mesenteric vascular system should not be ligated, as it would lead to the patient’s death due to intestinal ischemia.

    6. Anastomosing healthy tissue: Non-viable tissue and surrounding epiploic appendages should be removed. Additionally, intestinal resection should be carried out in a tumor-free area. The anastomosis should be performed on the antimesenteric border (isolating the mesentery from the anastomosis area). Distal and proximal fistulas and obstructions should be excluded. Precise approximation of the mucosal edges, facilitating primary intention closure and reducing fibrosis, should be performed in hand-sewn anastomoses. For this purpose, the seromuscular layer should be meticulously approximated with relatively deep bites that include the submucosa (the strongest layer).

    7. Well-approximated intestinal stumps: A reference suture point at the distal end of both stumps will facilitate proper alignment during anastomosis. Before that, the type of anastomosis should be designed, whether end-to-end, side-to-side, or side-to-end, as well as the direction of intestinal flow, whether isoperistaltic or antiperistaltic. In lateral anastomoses, care should be taken not to leave a blind pouch.

    8. Ensuring an adequate lumen caliber: Avoiding stenosis, especially in jejuno-ileal anastomoses where the diameter of the intestinal loop is smaller, is crucial. In hand-sewn anastomoses, it should be ensured that both ends are homogeneous; otherwise, techniques can be used to correct this by spacing the bites on the larger side and tightening them on the smaller side. Preferably, 3/0 absorbable monofilament or polyfilament/barbed sutures should be used, through simple or continuous sutures, depending on the surgeon’s preferences. In the case of mechanical anastomoses, staples should be properly aligned with the angulation and the staple size required for the intestinal segment (Table 1).34

    9. Correct closure of the defect with adequate hemostasis: Hemostasis is essential for proper anastomosis consolidation. Moreover, angles of the anastomosis should be inverted to reduce the risk of leakage. As for closing the defect, it should be well-balanced, not too tight to reduce tissue perfusion and promote ischemia and necrosis, but not too loose, as it would increase the risk of leakage. Similarly, the defect can be reinforced with a second layer depending on the surgeon’s preferences.

    10. Anastomosis watertightness: The hermetic closure of the anastomotic ring should be evaluated in all anastomoses using the bubble test or by injecting methylene blue transanally. Similarly, in end-to-end mechanical anastomoses, the integrity of the donuts should be analyzed. In case of doubt, in addition to leaving a drain, a proctoscopy can be performed to inspect the staple line and assess the advisability of creating a diversion ileostomy. In this regard, special caution should be exercised in patients with additional risk factors (previous pelvic radiotherapy, close distance to the anal margin along with advanced age, low albumin, or additional intestinal resections).35

    Figure 2

    Mobilization of sigmoid colon and transection of proximal stump using GIA stapler.

    Figure 3

    Preparing the rectum and transection of distal stump using TA stapler.

    Figure 4

    Anastomosing the bowel, checking the tissue donuts, and testing anastomosis watertightness.

    Table 1

    Dimensions of commonly available staple cartridges used to accommodate different tissue thicknesses for appropriate tissue management

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    References

    Footnotes

    • Twitter @Quique_ChC

    • EC and LC contributed equally.

    • Collaborators Dr Chiva was responsible for the planning and design of this review article. Dr Chacón conducted the research and wrote the article.

    • Contributors Drs Chacón and Chiva both specifically contributed to the planning, implementation, and communication of the work described in this review article.

    • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

    • Competing interests None declared.

    • Provenance and peer review Commissioned; externally peer reviewed.