Head and neck cancer and its treatment: historical review

BRITISH JOURNAL OF ORAL & MAXILLOFACIAL SURGERY

British Journal of Oral and Maxillofacial Surgery (2000) 38, 209–220© 2000 The British Association of Oral and Maxillofacial Surgeonsdoi:10.1054/bjom.1999.0273

Head and neck cancer and its treatment: historical review

M. McGurk,* N. M. Goodger†

*Professor; †Lecturer, Department of Oral and Maxillofacial Surgery, Guy’s Hospital, London UK

SUMMARY. Head and neck cancer has been known to physicians since antiquity, but until relatively recently anymaterial advance was limited by the lack of anaesthesia. The factors and people that helped to develop the subject ofhead and neck surgery have been traced through history, and this paper provides a broad historical perspective withwhich to compare the current standard of management for head and neck cancer.

Fig. 1 – John Hill MD (Courtesy of the Wellcome InstituteLibrary, London).

Head and neck cancer is not a modern disease; defectsin the skull base indicative of nasopharyngeal carci-noma have been described in Egyptian skulls datingfrom 3000 BC,1 and Moodie reported a range of jawand skull tumours in prehistoric Peruvians.2 Oralcancer was not definitively described until the 17thcentury, but Hayes Martin thought that there were anumber of veiled references in ancient manuscripts.3,4

Cancer was perceived as an uncommon conditionpossibly because of the short life-expectancy, and onenotable 17th-century surgical text devoted only one-twentieth of its contents to malignant tumours.5

The therapeutic approach to cancer in the first andsecond millennium was dictated by Galen (150 AD)who explained cancer as a disease of one of the fourhumours of the body. His authority was such that forthe next 1500 years cancer was perceived as a systemicdisease, and the consequence was to discourage localin favour of general treatment.

In the 17th century, medical knowledge was gradu-ally illuminated by scientific discovery. After learningabout the newly discovered lymphatic system,Descartes (philosopher–mathematician–physician)replaced Galen’s ‘black bile’ theory with a mechanisticlymph theory, which ultimately led to the concept oflymph-node dissection, which is the cornerstone ofcurrent management.

Against this background of enlightenment, theopinions of two prominent physicians of the age,Sennert and Zacutus Lusitanus, had a detrimentalinfluence on the treatment of cancer. They proposedthat it was a contagious disease. This may seemincomprehensible today but must be viewed in thecontext of medical knowledge at that time. Physicianswere unable to distinguish between cancers andchronic ulcerative conditions such as tuberculosis orsyphilis, and this persisted until the turn of the presentcentury. The effect of this incorrect supposition wasto exclude patients from many hospitals up to themiddle of the 18th century.

AETIOLOGICAL FACTORS

A number of factors have been incriminated in theinduction of oral cancer.6–9 Syphilis was probably

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included because it was relatively common and, per-haps more importantly, a syphilitic taint was oftenblamed when other causes could not be found. Butlinreported that only a few of his patients with lingualcancers tested positive for syphilis despite the fact thatthe infection was reported to afflict one-third ofpeople admitted to London hospitals in the 19thcentury. Channing Simmons10 likewise reported thatonly 14% of his patients in Boston had a positiveWassermann reaction. Controlled studies by Fry et al.suggested a small added relative risk of approximately2.5%–3% in patients with syphilis.11,12

Tobacco was first brought to public attention bythe explorers of the New World and was widely usedin the court of France by 1562.3 This fashion was notaccepted by everyone, papal bulls were issued against

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Fig. 2 – An ecraseur.

it, and James I urged his subjects to avoid a ‘customelothsome to the eye, hatefull to the nose, harmefull tothe brain, dangerous to the lungs and in the blackestinking fume thereof, neerest resembling the horriblestigian smoke of the pit that is bottomlesse’.13 Thiswas accompanied by restrictions on the productionand sale of tobacco and a heavy tax on its use. InRussia, its consumption was punished by amputationof the nose and in the Swiss canton of Berne it rankedin the table of offence next to adultery.14 The use oftobacco grew despite these threats, however, and by1614 there were 7000 shops selling it in Londonalone.13

Tobacco first implicated as a cause of cancer in1761 by John Hill (Fig. 1).13 He wrote, ‘with respect tocancers of the nose, they are as dreadful and as fatalas any others … It is evident therefore that no manshould venture upon snuff who is not sure that he isnot so far liable to a cancer: and no man can be sure ofthat.’ Later in that century, in 1775, Sir Percivall Pott’sobservations on cancer in chimney-sweeps werepublished and Sömmerring in 1795 mentioned pipesmokers and cancer.15,16 Smoking was the preserve ofmen, and the pipe was the primary way of takingtobacco. In the 18th century, snuff supersededsmoking among the elite, and it was not until the Boerwar that cigarette-smoking became a habit thattranscended class.

Tobacco was alleged to lead to drinking, but ourSaxon ancestors were notorious drunkards longbefore tobacco was available. In London, theestimated per capita consumption of beer and spiritsin 1700 was strong beer 512 bottles, small beer 307,and spirits 4.7.17 Drinks other than alcohol were fewin the London of the 1660s, as water was regarded asdangerous. In Pepys’ time, wine was drunk as freely asbeer at every meal, and France was still the mainsupplier, principally of clarets.

Alcohol has been part of most cultures throughoutthe ages but curiously it was the Arabs who perfectedthe art of distilling in AD 800–900. Spirits were said tohave been brought back by soldiers returning fromwar in the low countries, and by late in the reign ofElizabeth I (1558–1603) they were consumed insufficient quantities to be taxed.3 By 1621 there were200 strong-water houses in London, mainly selling aspirit made from fermented grain called ‘aqua vitae’.

PRE-MODERN ERA (1500–1900)

Intraoral tumours

For centuries, it has been widely appreciated that largeportions of the tongue could be removed withoutundue threat to life or function, as shown byHunerich, King of the Vandals who cut out thetongues of the Christians in North Africa in 484 AD.18

Marchetti, Professor of Surgery at Padua in theearly 1700s, is credited as one of the first to remove alingual cancer, which he did with cautery.19 However,by 1800 the knife seems to have superseded cautery.20

Intraoral surgery

Surgical progress was not matched by developmentsin anaesthesia, and pain was a reality that lead aFrench surgeon in 1774 to state ‘il n’est pas exercé pardes hommes timides’. However, the patient writhing inagony was not the whole problem, but rather thethreat of uncontrollable bleeding. Large vessels werecaught and tied but general oozing was arrested byhot irons, packs, and the application of caustics ortincture of iron. The practice of ligating the arterythat fed the tumour before undertaking the mainoperation was introduced by Louis in 1759,21 but thecontinuing threat of exsanguination encouraged thesearch for new, less dangerous techniques. Slowstrangulation of the tumour by encircling it with a lineof sutures was reported by Home in 1805,22 and adevelopment on this theme was ecraseurs (Fig. 2),which were introduced by Bell in the middle of the

Head and neck cancer and its treatment 211

Fig. 3 – Two ecraseurs could be used together to treat largetumours of the tongue.

Fig. 4 – Routes of access for resection of intraoral tumours: 1,Jaeger 1831 (Maisonneuve described bilateral incisions); 2, Roux1836; 3, Regnoli 1838; 4, Billroth 1862; 5, Langenbeck 1875.

Fig. 5 – A submental approach to the floor of mouth (Regnoli1838).

19th century.18 Two ecraseurs could be used together(Fig. 3) and Boyer stated that with this device it waspossible to ‘remove the anterior portion of thetongue, the whole, the lateral half, or any tumourwhich developed on the superior or inferior surfaces

in the angle formed by the base of the tongue and thefloor of the mouth’. In 1854, Middledorpf added agalvanic current, which heated the coil and in theoryat least combined the advantages of cautery andcrushing.23

Transoral surgery

It was soon recognized that the intraoral route gaveinadequate access and, by the early 1800s, theRabelaisian characters of modern surgery wereexploring more complicated routes of access (Fig. 4).In this heroic age, one can only admire the stoicism ofthe patient and the emotional fortitude of the sur-geon, but it should be appreciated that these were notcommon procedures but noteworthy events practisedby only a few surgeons, and then only rarely. Sedillotdescribed splitting the lower lip and jaw in the mid-line,3 still without anaesthesia. Regnoli in 1838 useda submental approach to the floor of the mouth(Fig. 5). 24In 1831, Jaeger first described splitting thecheek25 and Maisonneuve took matters even furtherby splitting both cheeks.26 Billroth appreciated theimportance of good access and took the procedure astage further, removing a section of the mandibularbody to reach the tongue and oropharynx, wiring thebone back into position at the end of the proceduresimilar to today.27 Evidence that more difficult caseswere being tackled is provided by Bernard vonLangenbeck, who in 1875 resected the ramus of the

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mandible in continuity with the primary tumour.28 Ingeneral the results were disappointing; Pembertonwrote, ‘Under the best aspects the treatment of cancerof the tongue by operation can be looked at only as apalliative measure, the tendency after all operative,interference, however may well considered being to aspeedy relapse’.29 Tonsillar tumours were approachedwith similar trepidation as illustrated by the case ofGeneral Ulysses S. Grant.30

Anaesthesia in the form of ether was introduced in1847, and chloroform in 1849. Before this, the patientwas held by the surgeon’s assistants, or tied down, andalcohol may have been used, although this is notrecorded.31 Even when anaesthesia was available, itwas often not used because ‘its use in operations ofthe mouth is a vexed question’, with both surgeon andanaesthetist fighting for a share of the airway. In casesof severe haemorrhage, the patient was likely to awakefrom the anaesthesic. In the latter years of the 19thcentury, the problem of the airway was improvedwhen the Trendelenberg cannula was used through atracheostomy. Anaesthesia was an obvious advantagefor the patient but its effect on surgical practice wasmore subtle, and ultimately more important. Thesurgeon was gradually released from the stricturesimposed by time, and the relationship between carefultechnique and improved outcome was soon apparent.

Maxillary tumours

Like intraoral procedures, surgery of the maxilla wasrarely attempted before 1800. There is mention ofpartial removal of tumour by Wiseman,5 and a fewfurther references to such operations can be found,but not in surgical texts.31 From 1800 onwards, therewere attempts at local removal of such tumours,usually by raising skin flaps and local curettage. It isthought that maxillectomy itself developed about1820 and is recorded as first being done by Lizars in1826.32 By the second part of the 19th century, theoperation was established within Europe. Variousfacial incisions were recorded, the classic lateral nasalincision being first described by Gensoul32 and theinfraorbital limb is attributed to Blandin byFarabeuf.33 During the latter part of the 19th century,the procedures were refined, and by 1902 the lateralrhinotomy was described by Moure for treatment ofthe nasal cavity and ethmoids.34 The palate wasrestored by obturation from the earliest days, and thetechnique was well established by the beginning of the20th century.

Laryngeal tumours

No clear concept about how to manage laryngealtumours existed before the 19th century. It is difficultto imagine the problems encountered by the earlylaryngologists, because before the introduction ofcocaine in 1884 the larynx was hidden from view andprotected by forceful reflexes, which made adequateexamination impossible. The customary method ofexamination was with a finger used with great speed

and dexterity; the mucous membranes were paintedwith bromide of potassium, or solutions of morphia,chloroform, or ether (none of which proved to be asuccessful surface anaesthetic) and often the patientwas simply instructed to suck small pieces of ice for 15or 20 minutes before examination. There were somesurgeons who could apparently identify vocal cordparalysis manually,35 as well as lesions of the pharynxand epiglottis. Diagnosis was a subjective exercise, asbiopsy was unheard of until instruments were madeto facilitate the evolving technique of laryngoscopy.

The first authentic attempt to examine the larynxwas by Leveret in 1743 with a bent mirror comple-mented by a snare for removing polyps. ManuelGarcia, a singing teacher in Paris, popularized thetechnique of indirect laryngoscopy with a dentalmirror (this new product had been one of the failuresof the London exhibition of 1851). With a long-han-dled dental mirror and an accompanying hand mirrorhe was able to examine his own larynx at will becauseof the tremendous control he could exercise over hispharyngeal muscles. He communicated his findings tothe Royal Society in 1855.36 Further refinements wererequired before the technique was widely adopted; anartificial light and a concave mirror, first held in theteeth were described by Czernak, and placing themirror on a head band with a ball and socket joint tofree a hand for manipulation of instruments was pro-posed by Walker in 1864. The great exponent wasMorrel MacKenzie, who learned the technique ofindirect laryngology in Vienna and then returned tointroduce the new specialty of laryngology toLondon. He founded the Throat Hospital in GoldenSquare, Soho. At this Sir James Paget remarkedderisorily that ‘someone should start a hospital forDiseases of the Great Toe’. One of the effects of thisnew interest in laryngology was that more tumourswere recognized. In previous centuries, only a scorehad been described whereas more than 1000 werereported in the two decades after the introduction ofindirect laryngoscopy. The important laryngeal dis-eases of the 18th century were tuberculosis, diphthe-ria, and tertiary syphilis, as illustrated by FrederickRyland’s Diseases and Injuries of the Larynx andTrachea, published in 1837. This had a lengthy discus-sion on inflammation and only eight of the 328 pageswere devoted to tumours.37

Laryngofissure

In 1810, during the Napoleonic wars, Desault sug-gested an operation to split the larynx (laryngo-fissure) to remove trapped foreign bodies.38 A succes-sion of surgeons subsequently used and developed theapproach; Brauers of Louvain in 1833 divided thethyroid cartilage to cauterize a growth, and GordonBuck of New York used it in 1851 for treating laryn-geal tumours.39 Statistics collected in 1879 showedthat the results of 19 thyrotomies on 15 patients withcarcinoma of the larynx were poor, and only twopatients survived longer than a year. The importanceof laryngofissure was that it raised the possibility oflaryngectomy.

Head and neck cancer and its treatment 213

Fig. 6 – Theodore Billroth 1829–1894 (Courtesy of the WellcomeInstitute Library, London).

Fig. 7 – Theodor Kocher 1841–1917 (Courtesy of the WellcomeInstitute Library, London).

Laryngectomy

As early as 1829, Albers of Bonn experimented withlaryngectomy in dogs40 and a systematic study of thesubject was undertaken by Czerny41 in Billroth’s clinic.At operation, on New Year’s Eve 1873 (a contrast initself with todays Health Service), Billroth (Fig. 6)undertook the first successful laryngectomy (PatrickWatson of Edinburgh was reported to be the first todo a laryngectomy in a human but it was for syphilisnot cancer, and was not a true laryngectomy). Theoperation started as a laryngofissure but after thelarynx had been opened and found to be extensivelyinvolved with tumour, the patient was revived fromthe anaesthetic to give consent for a total laryngec-tomy. The procedure took 1 hour 45 minutes. Thetentative steps towards the standardized surgery oftoday had begun.42

In contrast, the results of early laryngectomieswere generally disastrous because of the complica-tions of fistulas, haemorrhage, shock, mediastinitis,and bronchopneumonia. The first disasters arosebecause the pharynx was left open and the tracheaunattached. The answer, appreciated by Gluck, was atwo-stage procedure. The first involved separating thetrachea from the larynx and suturing it to the skin toform a secure tracheostome. The larynx was removedtwo weeks later, which avoided the trachea and phar-ynx remaining in continuity after surgery with theinevitable complication of inhalation pneumonia. TheTrendelenburg inflatable cuffed tracheostomy tubestopped secretions entering the lungs, but it was oftenleft in position and not cleaned for days, which led to

local infection. Unfortunately, contemporaneous withthese developments, a widely publicized article by oneof the foremost laryngologists of the day, Solis-Cohen, appeared and reported a startling mortality of50% for laryngectomy.43 It was still an uncommonprocedure for, despite many more laryngeal cancersbeing recognized, only 108 operations were reportedbetween 1876 and 1886 with 21 cures. In retrospect, itwas not surprising that Mackenzie was reluctant toadvise that such an experimental procedure should betried on the Crown Prince of Germany. Not even thesurgeon was immune the dangers of this new opera-tion for, after his first laryngectomy, Professor FelixNager of Zurich feared for his life as a result ofthreats from the patient.

Despite these setbacks and early scepticism aboutthe procedure, Gluck and Sörensen persisted withlaryngectomy and slowly refined the surgical tech-nique to a single-stage operation with a well-formedtracheostome. Their work was recognized as the mostprogressive of the era and the last 63 of a series ofover 160 total laryngectomies were done withoutmortality.44

Thyroid

Theodor Kocher, professor of surgery in Bern (Fig. 7)and noted as a general surgeon, also practised andwrote on the topic of oral and pharyngeal cancer. Hewas reported to have treated 120 patients with lingualcancer, and was one of the first to take advantage ofthe advances in anaesthesia that allowed the develop-ment of meticulous surgical technique. In 1872,Billroth had abandoned thyroid surgery because ofthe great mortality from haemorrhage and sepsis.During his first two years in Bern, Kocher did 13thyroidectomies and in 1883 reported his first 100cases; 30 of these were total excisions and resulted in

214 British Journal of Oral and Maxillofacial Surgery

Fig. 8 – Burns showed the caustic effect of irradiation on the skin(from Coutard 1924 50with permission).

myxoedema. Billroth’s patients ironically had notdeveloped this complication. Kocher recognized theproblem, studied the evidence and thereafter avoidedtotal excision. He subsequently developed a largepractice in thyroid surgery, and in 1895 reported aseries of 900 thyroidectomies with an operative mor-tality of 1%. By 1898, a further 600 operations hadbeen added with only a single operative death and in1901 he recorded 2000 thyroid operations with anoverall mortality of 4.5%. This achievement should bejudged against the conditions of the day with noantibiotics, no fluid replacement, and the risk ofthyroid storm. Before this, thyrotoxic patients weretreated in stages by ligation of vessels, partialthyroidectomy, injection of boiling water, or stealingof the thyroid.45 The beneficial effects of preoperativeiodine were not reported by Plummer until 1923.46

Kocher received the Nobel Prize for his work onthyroid disease in 1909. This remarkable surgeon,with his careful, meticulous techniques, served as amodel for Halsted, who was studying in Europe at thistime.

Subsequently the leadership in thyroid andparathyroid surgery shifted to the USA as Halstedand his students adopted Kocher’s methods. Crile,Lahey, and the Mayo brothers founded their privatepractices largely on safe thyroid surgery. Perhaps a fit-ting epitaph to this period was captured in a lecturegiven by Cushing in 1913: ‘The accurate and detailedmethods, in use of which Kocher and Halsted were forso long the notable examples, have spread into allclinics – at least into those clinics where you or Iwould wish to entrust ourselves for an operation.Observers no longer expected to be thrilled in anoperating room; the spectacular public performancesof the past, no longer condoned, are replaced by thequiet, rather tedious procedures which few beyond theoperator, his assistants, and the immediate bystanderscan profitably see. The patient on the table, like thepassenger in a car, runs greater risks if he has a loqua-cious driver, or one who takes close corners, exceedsthe speed limit, or rides to applause’.47

The merit of careful meticulous surgery had at lastbeen recognized, yet nearly a century later the lure ofspeed still lingers.

THE MODERN ERA (1900–1990)

Radiation therapy

At the turn of the century, two important discoverieswere made at about the same time. On 30 November1895, Roentgen48 announced the discovery of X-rays,and in the same year Becquerel reported the phenom-enon of radioactivity. These were followed by thediscovery of radium by the Curies in 1898.

Radiation therapy evolved through four phases.49

At first (1900–1920), it was governed by the conceptthat the effectiveness of radiation was reflected in itscaustic action on the skin (Fig. 8), so irradiation doseswere initially measured in HED (German initialsfor erythema skin dose and equal to roughly 1100

roentgens). The early physicians could be forgiven formaking this assumption because in that era treatmentinvolved brutal cautery or surgery with a similarvisual effect. In the second phase, the emphasis was onselective destruction of the tumour with an attempt topreserve local tissue, mainly influenced by the Frenchschool at the Institut Curie. The effect of variablessuch as time, size of tumour, and wavelength were rec-ognized. The third phase reflected an emphasis onaccurate planning of treatment with respect toanatomical fields and dosimetry, which was led by theEnglish school.50 Finally, as the full properties of radi-ation became known, its use became the more exactscience that it is today.

Initially, cancers of the larynx were treated withempirical doses, duration and fractionation as judgedby each practitioner. This persisted for three decadesuntil Coutard51 provided a more uniform plan oftreatment. The early machines operated at 50–100 kVand the long exposure times were impractical, but by1922 a 200 kV apparatus was available and in USA700–800 kV machines were in use by 1931. X-ray ther-apy, during the period up to 1940, played a secondaryrole to radium implants and teletherapy.

In Coutard’s technique, the duration of treatmentwas governed by the size of the tumour; smalltumours were treated in 15 days, medium ones in20–25 days, and large lesions with lymphadenopathyin 35–40 days. Interestingly, if treatment was less than

Head and neck cancer and its treatment 215

Fig. 9 – Radium salts suspended between the vocal cords bystrings.

Fig. 10 – Head devices for application of radium (from Cade 192963with permission).

20 days, a multifractionation (two fractions a day)technique was used (70 years later the method was re-examined by the Medical Research Council). Thechoice of case was important, but cures of 32% werereported for laryngeal cancers. The complicationsincluded oedema, and delayed osteoradionecrosis andchondroradionecrosis, which caused death by infec-tion and haemorrhage. In 1949 Baclesse, who suc-ceeded Coutard at the Curie Foundation in 1937,described three techniques: the first to avoid severeskin reactions; secondly, the shrinking field techniquebased on the premise that the centre of a tumour ismore resistant than its periphery (this required carefultopographical definition of the tumour); and thirdlythat larger lesions require higher doses for control. In1951, Baclesse reported the five-year survival rates of333 patients with cancer of the larynx, 17% between1919 and 1939, and 37% for those treated between1940 and 1946.

Curietherapy (radium therapy)

Radium therapy began when Becquerel and Curieentrusted some material to Dr Danlos at the St LouisHospital, Paris. Its progress was dependent on theavailability of an extremely limited amount of theelement. For therapeutic purposes, radium was used

in the form of a radium bromide and not as the puremetal. Initially, dermatologists were the mainchampions of the technique, producing plaques ofdifferent sizes covered with a special radioactivevarnish. The failure of topical treatment to treattumours within the body encouraged the applicationof radium directly on or in the tumour. The initialattempts were clumsy, with sausage-shaped bags con-taining radium salts being suspended between thevocal cords by strings threaded through the mouthand a tracheotomy (Fig. 9). Other cumbersome headdevices were also used (Fig. 10), as were surface appli-cators to irradiate the neck. Radon gas was a muchcheaper source of radiation than the salts, and in 1914Stevenson of Dublin described a method of loading aglass capillary tube filled with radon gas into a needlefor introduction into a tumour (the antecedent ofmodern interstitial iridium wire radiation). Interstitialtreatment until then had involved burying one or twotubes of radium (25 mg) in the tumour but the traumainvolved and the heterogeneity of the radiation fieldmade it unacceptable. The use of multiple needlessuitably placed offered the prospect of a more appro-priately delivered dose of radiation. Access to thetumour required surgical skill, and the first radio-therapists were accomplished surgeons. Radium treat-ment therefore took two forms; firstly, the applicationof needles that contained varying amounts of radiumsalt in platinum-lined tubes52 (the platinum wasimportant as it absorbed all the unwanted α andβ radiation) and were removed after a period.Secondly, radon seeds were used, and as the radon gaslost its radioactivity at approximately 10 days, theseeds were left in place. Duane developed the tech-nique and published his work in 1917.53 Bare glassseeds were developed and widely used at MemorialHospital New York but, after experience of severetissue reaction and at Regaud’s suggestion, gold foilwas added, originating the ‘Gold Radon Seeds’.54

Initially interstitial radiation was not used in thelarynx but the poor results of the intra-cavity treat-ment using suspended bags forced a reassessment. In1923, a combined surgery–radiotherapy approach wasintroduced by Ledoux in Brussels who fenestrated the

216 British Journal of Oral and Maxillofacial Surgery

Fig. 11 – Radium needles were placed against the perichondrium(from Cade 1929 63with permission).

Fig. 12 – Sir Henry Butlin 1845–1912 (Courtesy of the WellcomeInstitute Library, London).

thyroid cartilage to allow needles to be placed into thetumour so reducing cartilage necrosis. The techniquewas improved by Finzi and Harmer,55 who just laidthe needles against the perichondrium rather thanpiercing it, but the method was not widely practisedbecause of lack of materials (Fig. 11). Tonsillartumours were treated by exposure of the ramus of themandible through a submandibular incision (underlocal anaesthetic). Bone was removed with rongeursand needles were placed deep to the tumour on thepharyngeal wall.56

Telecurietherapy

It was not until the advent of telecurietherapy in1925–35 that radiation therapy of the larynx becameroutine. Telecurietherapy may be regarded as treat-ment with X-rays in which the radiation is providedby a radioactive isotope. The primitive form oftelecurietherapy consisted of a radium collar; non-treatment surfaces were lead lined and the radiumsource maintained at a distance of 5 cm from thepatient by cork or wooden slats. This had the dis-advantage that much of the radiation was absorbedby the superficial tissues and, because it was poorlydirected, it posed a risk to patient and staff alike. Theearliest types of apparatus produced a cloud of radia-tion rather than a beam and consisted of a boxweighing 150 lb suspended from the ceiling controlledby a series of pulleys. The box was lead-lined and hada window to allow the radiation to escape. A colum-nated beam was required. In 1919, a 5 g radium bomb(a large quantity of radium in a single container) wasplaced at the disposal of the Middlesex Hospital,London, and the radiation delivered from a box likeapparatus. The results were poor. Subsequently, 4 g of

radium was placed at the disposal of the WestminsterHospital to be used as a single unit housed in a bell-like container. In 1933, Sievert described a machinethat would allow treatment of head and neck cancer57

and this was improved on by Grimmett and installedat the Royal Marsden, London, in 1936.

Technical advances made cobalt and 2 MeVgenerators available in the 1950s and more recentlylinear accelerators and neutron beam therapy haveeclipsed cobalt in modern practice. The final develop-ment that has only truly been realized during the lasttwo decades has been the marrying of surgery andradiotherapy to gain the optimum benefit from both.

MODERN SURGERY

The turn of the century

Modern surgery started at the end of the 19th century.The advent of sound pathological concepts, the intro-duction of anaesthesia, and Kocher’s championing ofcareful technique showed that head and neck surgerywas possible without the previous appalling mortality.

Henry Butlin (Fig. 12) maintained the progressinto the 20th century. He had been appointed to StBartholomew’s Hospital in 1880 and, as the mostjunior surgeon, was offered the least popular clinicalpractice from which he fashioned a distinguishedcareer in the treatment of head and neck cancer thatculminated in a knighthood. Butlin remarked on hischoice of surgical career by relating that at StBartholemew’s the staff post to the throat clinic fellvacant and was discussed by the medical committee.Finally the senior surgeon who was the chairman said,‘Well Butlin is the youngest of us, he will have to doit’. So, said Butlin, he was thrust into a subject ofwhich he knew nothing.

His careful note-keeping and follow-up of patients(in 1898 he was able to trace all but seven of 102 hehad treated) showed that the treatment of oral cancer

Head and neck cancer and its treatment 217

Fig. 13 – George W. Crile Sr, 1864–1943 (Courtesy of theWellcome Institute Library, London).

was not as hopeless as suggested by contemporaryresults (5% cure in 1883).58 In his hands, cure wasobtained in about 28% of patients. It was alsoapparent to him that at least 30%–40% of patientswho were treated successfully for their primary lesionsuccumbed to nodal metastases. He therefore pro-posed and practised a nodal dissection of the anteriortriangle of the neck.58,59 Today this has been reintro-duced and has found favour as a modified or selectiveneck dissection. In 1909, on his retirement, Butlinanalysed 200 lingual cancers treated during his 25years in practice, and reported a cure in the latter partof the series of 41.5%. In the USA, his contemporaryGeorge Crile Sr (Fig. 13) also realized the importanceof nodal spread, suggesting that the problem waswidely appreciated by the surgeons who treated thesepatients. Although the relevance of node dissection incancer had been raised by Halsted (regarding thebreast), it was Crile who took the concept to its ulti-mate conclusion in the head and neck, and in 1906published his classic description of radical neck dis-section based on 132 operations.60 Crile had a particu-larly innovative mind, and his operation wasintroduced in an era where there were no intravenousfluid replacement, or antibiotics, and poor control ofthe airway. He dealt with the anaesthetic problems ini-tially by operating under local anaesthesia, but helater used nasopharyngeal intubation with the tubeheld above the larynx, and the pharynx packed toavoid inhalation of blood. Sepsis was reduced by dis-secting the neck as a separate procedure a month afterthe primary resection in the mouth or pharynx,thereby avoiding contamination of the neck by oralfluids. To limit the incidence of shock, he used a rub-ber pressure suit to maintain the central circulationduring the operation, an ingenious invention that hasrecently been reintroduced in emergency medicine asthe ‘shock suit’.60

Despite these advances, surgery was a desperateaffair plagued by complications the most common ofwhich were delayed healing and failed treatment. Aslate as 1923, Billroth’s maxim ‘avoid suturing the floor

of mouth and seldom see severe sepsis or secondaryhaemorrhage’ was still being practised. With the risingpopularity of radiotherapy during this period, andagainst the unequal challenge of sepsis, fluid loss, andanaesthetic difficulties, surgery lost its momentum.Unlike the abdomen, the happy hunting ground of the‘general surgeon’, the face is not concealed behind acorset or waistcoat, and surgical excisions in the headand neck left major functional and cosmetic defects.There was also the fearsome reputation of thetracheostomy, which was related to bleeding. It wasthis fear, compounded by a convalescence that wastechnically described as ‘stormy’ that dissuadedsurgeons from tackling head and neck cancers.Despite the fact that, in the UK there were manycapable general surgeons during this period, onlyTrotter took an interest in the field of head and necksurgery.

Against its primitive backdrop must be laid thenon-invasive, almost mystical action of radiation,which was perceived as the ‘Holy Grail’ for cancertreatment. Sir Stanford Cade pointed out that‘surgical treatment in the hands of conscientious andskilled surgeons has given results so indifferent thatthose obtained by radium appear brilliant’.61 In theUSA, Quick, representing the Memorial Hospital,New York, extolled the virtues of radiotherapy andparticularly the radium implant developed by HenryHarrington Janeway (an accomplished surgeon whostudied the physics of radiation). Surgeons still pre-ferred to remove early cancers, for instance TI tongueor early cord lesions, but any lesion that required asubstantial resection was gladly handed over to theradiotherapists.

By 1920, many of the teething troubles withradium had been overcome. Every large hospitalstruggled to obtain a supply of material and becauseof its rarity special departments started to develop.Initially the general surgeons nominated one of theirnumber to handle the radium cases: Stanford Cade atthe Westminster, Douglas Harmer and Finzi at StBartholomew’s and Mount Vernon, Ralston Patersonat the Christie Hospital, and Douglas Lederman atthe Marsden Hospital (Royal Cancer Hospital).Radiotherapy units blossomed and developed intodistinct departments ultimately with their ownpremises by the late 20s or middle 30s. Between 1920and 1940, radiotherapy dominated the managementof malignant disease in the head and neck, asillustrated by Cade’s book on radiotherapy, a third ofwhich was dedicated to the head and neck.62

Radiotherapy evolved so rapidly that no trainingpathway was designed until the 1950s although, by1943, a diploma (DMRT) could be obtained. Duringthis period, new surgical fashions blossomed thenwilted. Electrosurgery was thought to be a greatadvance in the treatment of head and neck cancer andwas championed by Harmer and Paterson. It wasused to reduce tumour bulk, particularly in themaxilla, by what amounted to opening of the cavityand electrocurettage, and was followed by intracavityradium applied by dental obturators.63

218 British Journal of Oral and Maxillofacial Surgery

Fig. 14 – Hayes Martin 1892–1977 (Courtesy of the MemorialSloan-Kettering Cancer Center).

The Resurgence of Surgery

By 1923 the initial enthusiasm for the new panaceawas already waning for it was recognized that smallcancers were eminently curable by surgery.Radiotherapy was used to treat neck metastases, butthis practice was soon recognized to be unproductiveand, as early as 1928, Cade was advocating surgery.Against the general euphoria for radiation therapysome protagonists of surgery existed; V. P. Blair ofSt Louis continued to advocate surgery and remarkedthat ‘cancer is best handled as if it were a skunk – let italone or kill it quick, only grief can come from irritat-ing it’.64 These sentiments might be presented morearticulately today, but with less impact, as ‘the firstcourse of treatment gives the best prospect of cure’.

Hayes Martin (Fig. 14), a radiotherapist andgeneral surgeon at Memorial Hospital, New York, inthe early 1930s, had focused on improving cure ratesby treating the primary tumour with X-rays by theCoutard method supplemented with gold radiumseeds. The radiation was not restricted to the primarytumour as the neck was also treated and persistentdisease managed with a block dissection ‘under localanaesthetic’ – an experience exhausting for surgeonand patient alike. In 1939, Martin undertook a surveyof the results of treatment of carcinoma of thepharynx, a standardized recording system havingbeen introduced in about 1934. The Memorial resultswere modest compared to the claims of other institu-tions. Their survival for patients with a pharyngealcancer was in the region of 5%, or 95% failure.65

Martin became slowly disenchanted with the resultsand became a proponent of radical surgery. Thischange in attitude coincided with a number of allieddevelopments which collectively were a major asset tothe surgeon and reduced the risks of a major opera-tion. Improvements in anaesthesia with the introduc-tion of pentothal and curare allowed routineendotracheal anaesthesia with a reduced risk ofaspiration. Blood replacement became available andhypovolaemic shock compounded by dehydrationbecame a thing of the past. The commercial produc-tion of sulphonamides in the 1930s and penicillin inthe 1940s made it possible to counter infection, andMartin was able to reintroduce the concept of acombined neck and oropharyngeal approach. Thisbecame known at Memorial as ‘commando pro-cedure’ (from wartime commando manoeuvresinvolving an attack from two directions).66

As a direct result of the World War II, interest wasrekindled in reconstructive procedures that had previ-ously been forgotten, and this complemented therevival of surgery in the management of head andneck cancer. The use of a split skin grafts had beenfirst introduced in 1917 by Esser and, in the same year,he described an axial pattern flap based on the tempo-ral artery.67,68 Blair introduced regional flaps in 192569

and these were later popularized by Egerton,70

Mcgregor71 and Millard.72 These were the antecedentsof the deltopectoral flap popularized by Bakamjianand Littlewood.73 Martin was therefore able to pursuea policy of radical surgery not available to his prede-cessors. Reconstructive surgery had come of age.

Gradually, the limitations that had been imposedon previous generations of surgeons were lifted. Oneconsequence was that the severe complications thatused to accompany this form of surgery and thatdeterred all but the most determined surgeon werereduced. The surgical discipline became more attrac-tive and a less daunting experience. In the USA, thetentative advances of ENT surgeons (such asBalantine, and Ogura) driven by their specialist know-ledge of the larynx into what was considered thedomain of the general surgeon, brought witheringattacks from Martin.74 This was not the case in theUK, where the practice of head and neck surgery hadbeen so completely abandoned by 1950 that there wasno critical mass of expertise remaining in generalsurgery and this discipline was no longer in theirrepertoire. The same applied in ENT. Surgery hadbeen so completely abandoned that after LionelCollege, who was one of the few ENT surgeons tocontinue practising laryngectomy during the radio-therapy era, retired in 1944 and his assistant SamBurdstal, who retired in the 1950s, the techniques hadto be retrieved from the USA. This fell to the ENTsurgeons. Henry Shaw was one of the first to visitMartin at the Memorial in the 1950s followed byWilliams in the 1960s. Stell went to Ogura at St Louis,and Shaheen and Harrison visited Iowa. The wheelhad turned full circle; the US surgeons were nowinstructing the Europeans as a result of the brief butprofound interaction between Kocher, Halsted andCrile 80 years previously.

Head and neck cancer and its treatment 219

In the latter half of this century other aspiringtreatments have been introduced, which then fadedfrom view. A major initiative of the 1970s and 1980swas cytotoxic chemotherapy, but the way that it wasapplied it offered little material benefit in terms ofcure when used as adjuvant or neoadjuvant therapy inadvanced disease. However, there is currently a resur-gence in its use for organ preservation. The prospectof improved radiotherapy results was also raised bythe introduction of hyperbaric oxygen and radiosensi-tizers, but to little effect. More recently, the introduc-tion of neutron beam therapy (which is not dependenton oxygenation of the tissues, a factor held respon-sible for failed radiation) offered the prospect of abreakthrough in non-invasive therapy. Unfortunately,the initial results could not be substantiated.

There has been little advance in surgical techniquesfor resection of tumours, other than the establishmentof craniofacial resection of lesions of the paranasalsinuses. However, reconstructive techniques havegradually improved with the advent of free vascularflaps and continued with osseointegrated implants,which produce vastly improved cosmetic results.

The evidence that has accrued over the last 100years suggests that current treatment regimens, inappropriate hands, are approaching their curativepotential. Multidisciplinary therapy is now the norm.Patient’s expectations have produced a sympathy forconservative and more selective surgical treatmentand clinicians have risen to the challenge, at the sametime trying to maintain or improve survival. The hopefor the future lies with the development and under-standing of the molecular basis of cancer. Until this isachieved, V. P. Blair’s statement remains pertinent:‘it is difficult to pick the incurable case and any proce-dure that gives a fighting chance is justifiable. Theother side of the picture is 100 per cent deaths, in theworst form known’.64

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The Authors

M. McGurk MD, FRCS, FDS, DLO, RCSProfessorN. M. Goodger BSc, MBBS, FDSRCSLecturerDepartment of Oral and Maxillofacial SurgeryGuy’s HospitalLondon, UK

Correspondence and requests for offprints to: Professor M.McGurk, Department of Oral and Maxillofacial Surgery, Guy’sHospital, London SE1 9RT, UK. Tel: +44 (0) 171 955 4342; Fax:+44(0) 171 955 4165

Paper received 22 August 1998Accepted 8 November 1999