Historical Outlook

THE AMERICAN PERSPECTIVE

It is acknowledged that the management of neck metastases from cancers in the upper aerodigestive system is very important to achieve a patient cure. Some form of surgery for removing neck metastases has been used for a century in the United States. During this period there was debate, dogma, and dissension. The issues included the kind of dissection, the timing of dissection, whether to dissect one or both sides, and whether to dissect in the absence of evidence of neck metastases. These issues remain unsettled today. As new treatment tools became available, questions arose as to their place in neck treatment. Radiation, with or without dissection, is still a debatable issue. The place for chemotherapy is undecided.

Crile and the Radical Neck Dissection

Crile identified several contemporary issues. He suspected a biological difference in tumor behavior and prognosis between patients who had palpable suspicious neck nodes and those who did not. He favored the radical operation for those who had palpable disease and a more limited operation for the others. The concept of a segmental or selective neck dissection is not new. Only the words used are new. Crile was not concerned about bilateral neck dissections, but he did note that staging was prudent. He believed that dissection in early cases in the absence of palpable disease was important. Increased rates of cure and decreased rates of recurrence occurred if the clinically negative neck was treated at the time of primary surgery. No statistics were cited to support his belief. Crile noted, without reference to the clinical situation (staging came much later), that among 48 patients who did not have a radical neck dissection, only nine were alive 3 years later. Of 12 other patients who underwent neck dissection 3 years after dissection, 9 were alive. From this he concluded that the radical operation was four times as effective as the less radical procedures (node picking or no neck treatment). This impression, with little supporting data, persisted for decades.

Hayes Martin and the Concept of Head and Neck Surgery

Head and neck surgery made little progress in the ensuing decades in North America. The various surgical groups interested in head and neck cancer acknowledged a need for a more focused effort. To this goal, a head and neck service was established at the Memorial Hospital in New York City in 1914. Similar services were not developed at other centers for many years.

The term head and neck surgery had very little meaning until Dr. Hayes Martin used it in the 1940s. Ward, Hendricks, and Martin initially defined the scope of the specialty. Training was limited to rotations on the Memorial Hospital service by general surgeons during a general cancer surgery program. Physicians who were exposed to and influenced by Martin supervised most surgical training in the following decades. General surgeons usually received the training, which meant that regional surgeons such as otolaryngologists and maxillofacial surgeons were limited in their experience with head and neck cases.

Martin had a profound influence on the direction and dogma of head and neck surgery. The radical operation was his standard. It was defined as an “operation that purports to remove, as thoroughly as possible, from the lateral and anterior aspects of the neck, the lymphatics (lymph nodes and lymphatic vessels) that are likely to be involved by metastatic cancer. The field of operation should begin above the lower edge of the mandible and extend to the clavicle below. Anteriorly the dissection should begin in the midline and be carried posteriorly to the anterior edge of the trapezius muscle. The procedure should include the removal of the sternomastoid and omohyoid muscles, the internal jugular vein, and the submaxillary salivary gland, en bloc.” The concept of partial neck dissection was acknowledged by Martin: “When the field is confined to specific limited portions of the neck, such as submaxillary area and supraomohyoid region, the term ‘partial neck dissection’ should be used.” Partial neck dissections include submaxillary dissection, dissection to the omohyoid muscle, and preservation of the sternomastoid muscle, internal jugular vein, and spinal accessory nerve. These more conservative operations were favored by some but not by Martin.

Martin’s indications for the radical operation were precise. He taught that

1. There should be definite evidence that cancer was present in the cervical lymphatics. This principle ruled out the so-called prophylactic or elective neck dissection.

2. The primary lesion giving rise to the metastases should have been controlled, or if not controlled, there should be a plan to remove the primary at the time of neck dissection.

4. There should be no clinical or roentgenographic evidence of distant metastases.

5. Neck dissection should offer a more certain chance of cure than radiation therapy.

Martin detailed the relative nature of the concept of fixation: “All fixation is not the same and some fixed nodes can be removed completely.” He also decried the term inoperable, which to him meant that the surgeon “lacks the confidence to complete a meaningful operation.” Martin did not teach prophylactic neck dissection. This axiom was based on statistical analysis of data from the Memorial Hospital, concluding that too few patients benefit from an elective procedure to justify its use. The absence of any statistical guidance as to whom might benefit from a prophylactic dissection led to the universal use of the complete or radical operation in therapeutic situations only. Martin decried “individualization” or “deciding each case separately” as “arbitrary decisions that were a matter of a physician’s state of mind and optimism or pessimism, which may vary from day to day and is based on the most recent experience.” He doubted that surgeons were capable of making decisions by balancing and weighing a set of dissimilar factors such as age, general health, primary site and size, economic status, and reliability, in a way that would have practical impact on the probability of survival: “Even though some members of the medical profession should actually possess such occult powers to select treatment methods in individual cases without reference to, or in regard to statistical evidence, nevertheless, such skills are surely limited in their usefulness and could hardly be taught to others.” This observation is still relevant today when we try to select and use the proper operation from a myriad of choices and combination therapy options and teach how to make these decisions to our students without statistical guidance. Martin was very clear on the goals of treatment. Survival without disease was the only worthy goal. This means living a long time and dying of some cause other than the treated cancer.

The inconsistencies in the dogma of therapeutic dissection were acknowledged. The choice of not doing a prophylactic neck dissection was judged a calculated risk, and the propensity of individual surgeons to have different tolerance to risk was acknowledged. Today, we have the same debate, in that individual surgeons have their own threshold for the likelihood of metastases for which they would recommend an elective neck dissection. Elective is the contemporary term for prophylactic because a neck dissection in the absence of proven disease prevents nothing. In Martin’s time, there was the subtle suggestion that a prophylactic dissection actually prevented something, but what that something was is not clear.

Another inconsistency noted was that bilateral prophylactic dissections were theoretically needed to be consistent with some primary sites treated. For practical reasons, bilateral prophylactic dissection was not a policy or practice of the Memorial Hospital Head and Neck Service.

The principle of radical neck dissection was to remove, as completely as possible, the structure of the lateral neck. The compromise nature of this axiom was obvious. Some structures cannot be practically removed, and others are removed at a functional cost. Structures in the same proximity to metastatic cancer, where the price of removal is too high to be accepted as routine, are the internal carotid artery, the vagus nerve, the brachial plexus, and, to a lesser degree, the phrenic, hypoglossal, and lingual nerves, and the cervical sympathetic. The accessory nerve was always considered expendable. The radical operation’s oncological premise was “the bigger the operation, the better the chance for cure.” Researchers in head and neck oncology have been gathering data and refining the concept of bigger being better. We are concerned that this premise might be incorrect, in that variables other than the physician’s actions can determine the probability of a cure.

I (LWD) trained at the Mayo Clinic and worked with Beahrs. Head and neck surgery was exclusively the domain of the general surgeons. As a young man, Beahrs had been a visiting clinician at Memorial Hospital and had observed Hayes Martin and his Head and Neck Service, although he did not train with Martin. Beahrs was a founding member of the Society of Head and Neck Surgeons and had organizational connections with Martin and his followers. Charles Mayo was referred to as the “head doctor” as the fledgling Mayo Clinic gradually subspecialized. Goiter was endemic in the Midwest, and Mayo treated thousands of patients with goiter over the years. Charles Mayo, Pemberton, and Beahrs were active thyroid surgeons. When surgery of the lateral neck was needed, Beahrs and others were called on to do neck dissections. Laryngology was practiced through a service called “Oral, Plastic Surgery, and Laryngology.” This unusual combination of interests evolved when colleagues Peter Lillie and Gordon New decided that Lillie should focus on mastoid surgery and New on laryngeal diseases. This was before there were specialty boards or recognized medical and surgical specialties. Mayo grew and space requirements separated Lillie and New. New moved to a different section and Lillie stayed. Each pioneer developed a department, the department staff developed training programs, and the training programs produced specialists. Laryngology became part of the Plastic Surgery Service. Oral surgery became an independent specialty at a different location. Individuals trained under the domain of plastic surgery were laryngologists at Mayo. This was the situation when I (LWD) started otolaryngology training. Otolaryngologists did operations through body apertures, like the ear canal and nostril, but only general or plastic surgeons could use a knife to cut through the skin to reach underlying structures. Total and partial laryngectomy were common procedures performed by the laryngologist–plastic surgeon. Interested otolaryngology residents were allowed to work with the laryngologist–plastic surgeons at a junior level and, later, at a more senior level. When required, the otolaryngology staff and residents would request the laryngologist–plastic surgeon to perform a tracheostomy on ear, nose, and throat patients.

Only a few of the plastic surgeons were interested in laryngology. Kenneth Devine and John Lillie (Peter’s son) were both trained in general surgery. They became the primary laryngologists through the 1950s and 1960s and into the 1970s. Lillie had otolaryngology training, and Devine had additional plastic surgery training. No Mayo staff otolaryngologist had an interest or training in laryngology. The volume of otology and rhinology that passed through the Otolaryngology Service was such that there was no incentive to seek additional work. Head and neck surgery was an orphan interest with responsibility divided between the plastic surgeon–laryngologists and the thyroid surgeons. The thyroid surgeons did the neck dissections, and the plastic surgeon–laryngologists surgically excised the primary tumors. In practice, this meant that the thyroid surgeon saw the patient briefly in the office of the primary surgeon and would examine the patient’s neck, but not the primary tumor unless it could be seen with a tongue blade. The thyroid surgeon would agree that the neck should be dissected, with little concern about the primary or its metastatic probabilities. In the hospital, the thyroid surgeon would come to the operating room of the laryngologist, do the neck dissection, and leave, never to see the patient again. This arrangement continued for decades. Otolaryngologists at Mayo did not perform regional cancer surgery. Patients who arrived at the Otolaryngology Department with a head and neck cancer were transferred to the plastic surgeons.

These national trends were recognized at the Mayo Clinic. As otolaryngologists throughout the country gained respectability and the public recognized their role in managing regional cancers, the tertiary referral for patients with head and neck patterns gradually shifted at Mayo to the Otolaryngology Department. To accommodate the referral pattern, the laryngologists moved from the Plastic Surgery Section to Otolaryngology. The relationship with general surgeons in regard to neck dissection remained for a time. The laryngologists saw the patients, and a treatment plan developed. The general surgeons did the neck dissections. Follow-up and rehabilitation were managed by the laryngologist. New otolaryngologists with training in head and neck surgery did their own neck dissections. Gradually the general surgeons who did the neck dissections retired, and the cancer surgery for metastases to the lateral neck became the responsibility of otolaryngologists with an interest in cancer. This trend also occurred throughout the United States at other medical centers.

In 1979, the American Academy of Otolaryngology was renamed the American Academy of Otolaryngology—Head and Neck Surgery (the separation from ophthalmology had happened earlier). Formal training in head and neck surgery became an integral part of the basic otolaryngology program. Fellowship training became more available. Future specialists in head and neck surgery and oncology will come from these fellowship-trained specialists. Core otolaryngology training in head and neck surgery reached its apogee in the late 1980s. The advent of so-called organ preservation programs, which depend on the combination of chemotherapy and radiation with surgery for salvage, has hampered and even crippled the basic otolaryngology head and neck training. In many established head and neck cancer training programs the surgery of head and neck cancer reverted to a salvage role. With fewer patients treated primarily with surgery, experience of modified and selective neck dissection is infrequent, as is laryngeal conservation surgery. These trends diminish the training opportunities for head and neck surgeons.

Understanding the vicissitudes of head and neck cancer management in the United States following World War II requires insight into the economics of medicine. Fees for services prior to World War II financed health care. Doctors and hospitals billed patients, and patients paid their bills. The union movement was strong in the United States after the war. Unions, through collective bargaining, negotiated health care benefits for their members. Employers paid for the workers’ health insurance. This introduced a third party into the fee for service system, but bills were paid without negotiation. The popularity of insurance programs gradually expanded to the nonunion sectors of the economy. The availability of financing and the American belief that “more is better” allowed the growth of therapy programs combining surgery with radiation. These programs aim at increasing rates of cure and decreasing the number of local and neck cancer recurrences. Such combined therapy programs are an important part of the neck dissection story. In recent decades, payers, usually businesses, demanded some control on the growth of health care costs that were rising as much as 20% per year. Medical costs included excesses fostered by the “more is better” attitude. The insurance companies, under pressure from the business payer, questioned the cost of medical care. Insurance companies began to negotiate with doctors and hospitals. An incentive was provided to doctors and hospitals whereby insurance companies directed large blocks of patients to the care providers who accepted their payment schedules. Doctors accepted these incentives to keep a patient base as did hospitals. Insurance companies gained an influential position in health care decisions. Managed care was an outgrowth of the insurance companies’ pressure. In managed care programs, fee for service (or “more is better”) is being replaced by the concept of capitated reimbursement. The doctors and hospitals are given a negotiated amount to care for patients who are members of a larger group. More was no longer better; more was expensive and a threat to the financial viability of the hospitals and doctors. Many economic innovations in health care delivery followed. Ambulatory surgery and home health care became necessities. Whereas a patient with a laryngectomy and neck dissection would stay in the hospital for up to 2 weeks during the fee for service era, now the patients are sent home with feeding tubes and drains in place in less than 1 week.

Modifications to Neck Dissection

From Martin’s time, surgeons recognized that the Crile operation was not always necessary and was unwarranted in some cases of head and neck cancer. For surgeons who favored elective or prophylactic and bilateral dissections, it was evident that the radical operation was excessive when no metastases were found in the neck. Many terms (e.g., modified, supraomohyoid, upper, midline) were used to describe these lesser operations. The nomenclature became confusing to teach and lacked standardization for reporting. The American Academy of Otolaryngology—Head and Neck Surgery convened a special task force to address the terminology problems. The group was tasked to (1) recommend terminology that adhered to the more traditional words as radical and modified radical, (2) define which lymphatic structures and other nonlymphatic structures would be removed relative to the radical dissection, (3) provide a standard nomenclature for lymph node groups and nonlymphatic structures, (4) define the boundaries for resection of lymph node groups, (5) use terms for neck dissection procedures that are basic and easy to understand, and (6) develop a classification based on the biology of cervical metastases and the principles of oncological surgery.