Whether considering the practice of bloodletting or the concept of balancing of the four humors, the practice of medicine dates back centuries to the time of Hippocrates. Early physicians managed what were considered to be internal diseases, giving rise to the term “internal medicine.” Conversely, due to the extreme morbidity and mortality associated with an operation, surgeons were restricted to the management of superficial or external conditions. Sir James Simpson, a prominent Scottish physician in the 19th century, famously stated, “A man laid on the operating table in one of our hospitals is exposed to more chances of death than the English soldier on the field at Waterloo.”1 It was not until the advent of antisepsis, antibiotics and the introduction of modern anesthetic techniques that the abdominal cavity could be approached with an acceptable degree of success. These innovations brought about a revolution in the field of surgery. In less than a century the practice of surgery transformed from one restricted to procedures of necessity to elective procedures including life-saving resections of malignant tumors.
From a historical perspective, surgical approaches to cancer existed far before the discipline now known as “Surgical Oncology.” The surgical treatment of cancer originated as an approach focused on radical and debilitating tumor resections and extended lymphadenectomies. These “bigger is better” procedures focused on removing all locoregional tissues including those with any potential local extension in order to eradicate all cancer cells and draining lymph node basins. Much has changed over the last several decades that has made Surgical Oncology an academic and evidence-based specialty. What has led to modern Surgical Oncology being the field it is today is the development of large prospective databases, the design and participation in randomized controlled trials, and the translational research that has ushered specialized and customized patient cancer therapy.
Historical reports of oncology date back to 1600 BCE taken from accounts of Egyptian writers that describe surgical techniques to treat a variety of disorders including solid tumors.2 Hippocrates, the namesake of our oath as physicians, initially had a negative view on surgical therapy for solid tumors and believed that surgery would actually worsen survival (approximately 400 BCE). Hippocrates also defined the term carcinoma “crab-leg tumor” and sarcoma “fleshy tumor.”3 Galen described cancer as a systemic disease in the 3rd century.4 The first mastectomy for breast cancer was reported by Lenoidas, a 5th-century Greek physician. More significant advances came in the 1700s when John Hunter, who many consider to be one of the Fathers of Surgery, detailed concepts that would apply to both surgery and cancer.5 LeDran in the 18th century proposed the lymphatic spread of breast cancer and that in early stages was a local disease that could be treated effectively with surgery.4 At the end of the 19th century, Halsted popularized the radical mastectomy and was able to achieve a very low local recurrence rate by extending the resection margins in the mastectomy proposed by von Volkmann.4
The emergence of general anesthesia and introduction of blood transfusion and antibiotics in the mid- to late 1800s allowed surgeons to develop increasingly complex and safer operations for extirpation of cancer, leading to the preeminence of surgery as treatment for malignancy. Although alternate modalities for cancer treatment such as radiation therapy became available early in the 20th century, these were often fraught with imperfect technology and toxicities, and frequently developed independently and often in opposition to surgical therapy. True multidisciplinary cancer care did not develop until much later.
Pierre Curie first suggested the use of radiation therapy for the treatment of tumors in 1901, and initially this modality was hailed as a safer alternative to highly morbid operations.6 The technology was espoused and advanced by many prominent cancer specialists of the day, most notably Dr James Ewing from Memorial Sloan Kettering, the influential director whose oncology society became the precursor of what is now the Society of Surgical Oncology. He believed it was superior for the treatment of cancer and under his influence the institution, including its surgeons, devoted itself to development of this modality in the 1920s and 1930s.7 Initial efforts with radiation therapy were limited by toxicity and side effects, but over time techniques improved, aided by the emergence of a distinct specialty of radiation oncologists committed to the advancement of radiation therapy for cancer. The popularity of radical surgery versus radiation for cancer would wax and wane over the next decade but a combined approach using both modalities had to await both improved technology as well as a cultural change in the community of cancer surgeons.
Although radiation was the first nonsurgical modality to be used for cancer treatment, the development of the first chemotherapeutic agents changed the landscape of cancer care almost immediately.8 The immunosuppressive effects of nitrogen gas on afflicted servicemen in World War II were first described in 1917. Pharmacologists Dr Alfred Goodman and Dr Lewis Gilman were tasked by the U.S. Office of Scientific Research and Development with studying possible therapeutic effects of chemical weapons, and in 1942 they teamed up with a thoracic surgeon at Yale University, Dr Gustav Linskog, to administer nitrogen mustard to a patient with refractory lymphosarcoma.9 Later in the decade Dr Sidney Farber developed the first folate antagonists for the treatment of children with acute lymphoblastic leukemia, and shortly thereafter 6-mercaptopurine was described.10,11 After initial skepticism the medical community embraced the concept of pharmacologic treatment of cancer and “chemotherapists” began to arise from a variety of medical specialties.12
Early successes were mainly in hematological malignancies, which had traditionally not been the purview of the surgeon. However as medical oncology emerged as a specialty, these drugs began to be applied to the treatment of solid tumors, with varying degrees of success. Dr Jane Wright at New York University developed methotrexate and in 1951, demonstrated remission in patients with nonoperable breast and skin cancer.13 The efficacy of 5-flourouracil in colon cancer and other solid tumors was reported by Heidelberger and his team at the University of Wisconsin a few years later.14 The radiomimetic effect of the alkylating agents paved the way for a complementary use of radiation and chemotherapy, and the early multidisciplinary approach to cancer care involving medical and radiation oncologists who usually advocated for nonsurgical treatment. In addition to the hematological malignancies, head and neck, and cervical cancers were among the first malignancies treated in this fashion.
The medical treatment of cancer also became applied to hormonally sensitive malignancies. Charles Huggins first reported on the effect of estrogens and androgens on metastatic prostate cancer in 1941, and surgical castration became part of the armamentarium of the cancer surgeon, as did oophorectomy and adrenalectomy for breast cancer.15 With the subsequent development of artificial estrogens, gonadotropin antagonists and later tamoxifen, the role of surgery was also diminished in the realm of hormonal manipulation for the treatment of cancer.
This compartmentalization of expertise was new to surgeons, who had a long history of availing themselves of any promising technique in their crusade against cancer. Radiation therapy was explored by a number of prominent surgeons in the early 20th century, and the earliest forays into brachytherapy were usually surgeon driven. Dr Benjamin Barringer inserted radium needles into the prostate transperineally in 1917, and four decades later Dr Rubin Flocks at the University of Iowa pioneered interstitial injection of colloidal solution of radioactive gold into the prostate during open surgery.16 In 1924, a London-based surgeon named Geoffrey Keene went against the prevailing Halsteadian ethic of the day and over the course of 10 years treated 327 women with radium needles in the breast without surgery, demonstrating results comparable to those published for radical mastectomy.17 For a time in the 1950s, when most medical oncologists were focusing on hematological malignancies, some surgeons incorporated administration of chemotherapeutic agents for solid tumors into their practice. This combined approach continues to be the model for modern-day gynecologic oncologists. However, the burgeoning complexity and sophistication of other modalities increasingly led to specialization within other disciplines.
The emergence of cancer specialists in these nonsurgical fields fostered both the establishment of surgical oncology as a distinct field within general surgery and the development of the cancer surgeon’s role as leader within the community. Surgeons had since the 1800s been the primary physicians in the treatment of cancer. However, although there were surgeons who focused their career on cancer, surgical oncology was not recognized as a distinct subspecialty in most academic and community institutions until the 1960s.18 It became clear that as these other modalities improved and expanded, championed by their respective specialists, surgical oncology had to define itself more clearly.
The shift in focus from separate and sometimes opposing disciplines to a cooperative team was also prompted by the emerging concept of adjuvant chemotherapy. The first reports of improved survival after surgical resection followed by chemotherapy came in the mid- and late 1970s for osteosarcoma, breast, and testicular cancer.8 Work by Dr Bernard Fisher with the National Surgical Adjuvant Breast Project and Dr Umberto Veronesi at Istituto Nazionale Tumori in Milan exploring the role of adjuvant and neoadjuvant chemotherapy and radiation in breast cancer treatment further underscored the need for a multidisciplinary approach to cancer.19,20 The surgical oncologist needed to be familiar with all methods of treatment in order to select the most appropriate single or combination approach, of which surgery was just one.
Although multidisciplinary management is now considered standard of care not just for cancer but many other forms of disease, this paradigm did not become established in medical practice until the later 20th century. In 1922, the American College of Surgeons founded a consortium of professional organizations from a variety of disciplines dedicated to improving survival and quality of life for cancer patients through standard-setting, prevention, research, education, and the monitoring of comprehensive quality care. The Commission on Cancer has since that time set many of the national benchmarks regarding multidisciplinary care.21 The first government supported cancer centers were created through the NCI in 1960 with an emphasis on interdisciplinary research and treatment.22 By 1989, a combined study of the National Cancer Institute (NCI) and American College of Surgeons reported that over 90% of hospitals with greater than 100 beds and 85% of the hospitals with less than 100 beds were utilizing a regular multidisciplinary tumor board.23 Surgical oncologists continue to maintain a leadership role not only in the management of these complex patients, but also in cancer research and clinical trials.
One of the most important innovations of modern surgery has been the incorporation of minimally invasive approaches to the abdominal cavity. Laparoscopy owes much of its history to innovations made in the field of endoscopy and the modification of these techniques to suit the needs of a surgeon. As early as 1805 Phillip Bozzini was using his leather-covered, vase-shaped Lichtleiter to perform cystoscopies on dogs.24 Unfortunately, his invention was labeled a toy by the prevailing medical authorities. Bozzini’s professional career never recovered and he died from typhoid fever soon after. It wasn’t for another 100 years that the idea of introducing an endoscope into an unopened abdominal cavity was developed by George Kelling.25 Kelling was interested in identifying less invasive methods for treating common pathology. During his time, gastrointestinal (GI) hemorrhage was often a fatal condition. With this in mind, Kelling performed celioscopies in a dog model using pneumoperitoneum to tamponade the GI hemorrhage. Ultimately, he felt the view was limited and did not pursue the technique further than his initial experiments. Hans Christian Jacobaeus was the first to attempt a “laparothoracoscopy” in humans. A contemporary of Kelling, Jacobaeus was a staunch supporter of laparoscopy. In his experiments, he worked almost solely on patients with ascites, evacuating the fluid and creating a pneumoperitoneum to perform explorations. Despite his success, his minimally invasive techniques were greeted with skepticism and indifference.25 For the next 70 years physicians would perform occasional exploratory laparoscopies for various conditions, but without any true therapeutic intent.
The surgical inertia resisting laparoscopic techniques finally began to change in 1980 when Kurt Semm, a German gynecologist, performed the first laparoscopic appendectomy.26 Despite successfully addressing numerous gynecologic conditions laparoscopically, his data was often criticized as impossible. When he completed the first laparoscopic appendectomy he was vilified by both gynecologists and general surgeons. A commentary in Medical Tribune went as far as to say, “Thanks to modern methods of anesthesia, laparotomy today no longer poses a problem. This is the only way for a surgeon to be able to view the entire abdomen and to direct his procedure accordingly”.26 Unhindered by the cool reception, Semm persevered in his efforts to promote this new technology. Five years later Erich Muhe incorporated Semm’s techniques when he performed the first laparoscopic cholecystectomy with his Galloscope. Much like his contemporary, Muhe’s description of an alternative method to treat a common surgical problem was met with disdain.27 Both men were widely condemned by their peers with one critic calling it “Mickey Mouse surgery.” Within 4 years, however, the technique was presented by Jacques Perissat at the Society of Gastrointestinal and Endoscopic Surgeons (SAGES) annual meeting. Shortly after, the French experience was published in the Annals of Surgery marking the change from a slowly evolving field to a revolution of surgical technology.28,29
Much of the initial opposition to the adoption of laparoscopy was related to concerns over safety, ergonomics, and applicability.30 Unlike today’s wide screen, high-definition systems that allow the surgical team to work as a single cohesive unit, early laparoscopies were characterized by poor optics, inadequate lighting, and the necessity of the surgeon to hunch over a camera and look through a single eye piece. It wasn’t until the advent of automated insufflation systems, safe electrocautery, and videolaparoscopy that the laparoscopic operation could mirror that of a typical team-oriented open approach.30 It was following these advances that the integration of laparoscopy in general surgery escalated. All over the world, surgeons were introducing novel technologies and new approaches to diseases. Almost immediately surgeons noted benefits to a minimally invasive approach including decreased time for convalescence, quicker return of GI tract function, a decreased hernia rate, and even a reduction in perioperative mortality.31,32 Unfortunately, there were also drawbacks to this universal implementation. There were issues with credentialing and safety with some surgeons offering the approach after only a weekend course. The result was a dramatic rise in complications rates, as noted by an increase of major common bile duct injuries with laparoscopic cholecystectomy.33,34
Notwithstanding this widespread fervor over the potential of laparoscopy, the field of surgical oncology was slow to embrace the paradigm shift. There were many issues that contributed to this skepticism. Coinciding with the advances in laparoscopic technology was a better grasp of critical care and anesthetic techniques. The result was that pathology that was previously considered inoperable was being treated with radical resections. Moreover, with the increasing emphasis on surgical outcomes the idea of compromising the integrity of an oncologic resection in the name of a smaller incision was nonsensical. There were also concerns that had not been addressed including the safety of insufflation and multiple port sites in the setting of malignancy. Early on, pneumoperitoneum was implicated as a potential etiology for tumor dissemination.35,36 There were also numerous reports of port site metastases from various GI malignancies following laparoscopic resections.37–39 Not until well designed, prospective studies were completed that many of these concerns were put to rest. Today, a minimally invasive approach is considered the standard of care for many GI malignancies. When considering the laparoscopy in the armamentarium of a surgical oncologist, there are several indications for the approach including staging, curative resection, and palliation.
It is clear that today’s surgical oncologist has a vast array of diagnostic tools at his or her disposal including advanced radiographic imaging and endoscopic interventions in addition to a traditional history and physical. With that said, there are still instances where a diagnosis is in doubt or the appropriateness of a curative resection is not yet established. The ability to utilize minimally invasive techniques to complete the evaluation of a malignancy is advantageous to both the surgeon and the patient.
There are numerous GI malignancies for which a diagnostic peritoneoscopy would be appropriate. Pancreatic cancer is the seventh most common cause of cancer deaths globally resulting in over 300,000 deaths worldwide in 2012 alone.40 Its propensity to present late and with advanced disease contributes both to its poor prognosis and the complexity of a therapeutic algorithm. Classically, a tri-phasic CT scan is the diagnostic and staging test of choice, providing approximately 80% accuracy for the prediction of resectability.41 In those instances in which the diagnosis or resectability is in doubt, a staging laparoscopy can be incorporated. A Cochrane database systematic review noted that up to 23 unnecessary laparotomies in 100 patients with pancreatic or periampullary cancer would be avoided with a diagnostic laparoscopy.42 Another retrospective study published in the Journal of the American College of Surgeons advocated for extended laparoscopic staging to all patients with radiographic localized disease.43 While there is no question that the information gleaned from a radiographic evaluation is valuable, as many as 11% will have occult disease only identified on exploration.
Gastric and gastroesophageal cancers account for over one million cancer-related deaths worldwide each year.40 Much like pancreatic cancer, they may present late with disseminated disease, precluding a curative resection. The European Organization for Research and Treatment of Cancer (EORTC) published consensus guidelines on the treatment of these malignancies.44 In both cases, the experts supported the selective use of a staging peritoneoscopy in those patients whom resectability has not been definitively established. In those patients who are noted to have locally advanced disease and are treated with neoadjuvant therapy, occult progression of disease exists in up to 7% of cases. The use of staging laparoscopy to avert an unnecessary laparotomy is a valuable tool for both patient and clinician. The current diagnostic tools available to surgical oncologist have vastly improved workup of GI malignancies. However, the use of minimally invasive surgery to more clearly define resectability and guide a patient’s care is a tremendous benefit to the care of this population.