Adenomatous tumours of the anterior foregut region showing the cylindroma pattern

248 T H E B R I T I S H J O U R N A L O F S U R G E R Y

ADENOMATOUS TUMOURS OF THE ANTERIOR FOREGUT REGION SHOWING THE CYLINDROMA PATTERN

BY HELEN RUSSELL CONSULTANT PATHOLOGIST TO THE CHRISTIE HOSPITAL AND HOLT RADIUM INSTITUTE, MANCHESTER

INTRODUCTION THIS study of the adenomatous tumours of the anterior foregut region is based upon the collection of tumours which, during the past ten years, have been filed under the headings ‘ adenomas’ and ‘ mixed adenomas ’ in the Pathology Department of the Christie Hospital in Manchester.

In this hospital tumours of the anterior foregut may reach the pathologist from various sources,

was decided, therefore, to restudy all the histological material combined with the clinical follow-up data.

No case was included in the series of which an adequate histological preparation was not available in the laboratory collection. This was particularly necessary in specimens from the ectopic sites from which biopsy material is more likely to be inadequate than from the large serous salivary gland sites. Any

FIG. z88.-Classification of 255 cases according to site and histological type.

FIG. z89.-Prognosis in mixed adenomas and cylindromas. Follow- up details of ten years’ cases (1944-53) compiled in 19%.

namely, the general surgeon and the otolaryngological, thoracic, ophthalmic, and dental units. The majority of the specimens are obtained from the sites of the large serous salivary glands, that is to say from the parotid and submaxillary regions j but as the years have passed the collection of adenomas from ectopic, or aberrant, sites has accumulated, and tumours from the palate, cheeks, floor of mouth, antrum, tongue, tonsillar region, pharynx, lacrimal gland, and the trachea and bronchi, have been seen. Sometimes several tumours from ectopic sites were received each year, but in the rarer sites only one in several years, and only one adenomatous tumour of the trachea was seen in ten years.

The review of the ten years’ collection was under- taken for two reasons ; first, because occasionally metastases had been received from cases in which the primary lesion had been included in the non- malignant, ‘ mixed adenoma ’ category, and, secondly, because members of the oto-laryngological unit were concerned with the unsatisfactory course and grave ultimate prognosis in some of the adenomas occur- ring in ectopic sites. At first it was assumed that inaccessibility of site was responsible for the grave prognosis in the unusually situated tumours, but more careful investigation showed that this idea was not tenable for reasons which will be given later. It

wastage of material from this decision was counter- balanced by the importance of seeking a true prognosis based upon histological pattern. No attempt has been made to assess the general incidence of these tumours, because the Christie Hospital patients are highly selected from a population of over four million people, and they are gathered together because of the centralization of radio-therapeutic plant in this region of England.

The following section will provide the data from this survey, which led us to separate adenomas showing the cylindroma pattern from those of the mixed adenoma group, and which indicated that cylindromas are commonest in the ectopic sites, and have a grave ultimate prognosis. They appear to arise in the ducts of the mucous, rather than serous, salivary glands. Their mode of spread is that of a rodent tumour, giving relentless local recurrences, and occasionally late distant metastases. The clinical aspect of some of these cases has been published already (Harrison, 1955). Their course is distress- ingly slow, and inoperable recurrences with survival for many years, without either gland or other metastases, are quite numerous.

The history of the subject is so confused that it will be dealt with in a later section rather than as an introductory paragraph.

A D E N O M A T O U S T U M O U R S O F A N T E R I O R F O R E G U T 249

of the cubical lining cells into small polygonal cells which have very little protoplasm. These small cells, of which the tumour consists, are about the size of the

MATERIAL AND ITS ANALYSIS ~~~i~~ the decade under review, Over five

thousand histological specimens of all types (the

region were reported upon, and among these the adenomas numbered 272. Of this total 204 were mixed adenomas, 51 showed the cylindroma pattern, 5 cases contained both these patterns, and 12 were

majority of them turnours) from the anterior foregut basal cells of the epidermis, but rounder, and as

FIG. 290.-Cylindroma pattern in tumour of lacrimal (By courtesy of Dr. E. K. Dawron.)

gland.

classed as ' other adenomas '. Table Z gives their distribution, sex incidence, and survival rate in 1954. This paper is concerned with the 256 cases of the first two categories in TubZe I , but it may be noted that those of the third category are too few for study, and those of the fourth category, ' other adenomas ', showing neither the mixed adenoma nor the cylindroma pattern, present unsolved difficulties in classification.

Figs. 288, 289 illustrate the distribution of the 256 tumours between the large serous salivary gland sites and the ectopic sites, and show that the cylindromas are commoner in the ectopic sites, and have a much worse prognosis than mixed adenomas in the same sites. The palatal tumours alone illustrate this well :-

Palatal tumours of mixed adenoma type = 18- of which 17 were alive and well in 1954 ;

Palatal tumours of the cylindroma pattern = 17 - o f which 7 were alive in 1954, and of these 6 were inoperably recurrent. These figures prove that inaccessibility of site is not responsible for the grave prognosis of the cylindromas, because the mixed adenomas of the palate have been treated successfully when compared with an equal number of cylindromas which were unsuccessful.

HISTOLOGY The histological diagnosis of the cylindroma

depends, as in most tumours, upon the recognition of a tissue pattern, rather than upon the shape and size of individual cells. Figs. 290-294 illustrate this pattern in its most characteristic forms, and Figs. 297, 298 show modified forms in the rare distant metastases, of which we have only four examples in the ten years' histological collection, although the incidence of metastases is probably much higher.

The tumour is essentially an adenoid structure, which appears to arise from dilated mucous gland ducts whose epithelium shows degenerative metaplasia

FIG. 291.-Cylindroma palate of two years' duration treated by radium mould and implant in 1938. Excision of hard palate for recurrence in 1950. Further operation for removal of tumour in antrum and nasal cavity in 1954. ( X 30.)

FIG. z9z.-Adenoma of bronchus (cylindroma pattern) residual after several operations over five years.

Krompecher pointed out, they are like the cells of many basal cell skin tumours. They are arranged around duct-like spaces or are packed closely within the spaces in columns and drifts of cells, and the spaces containing degenerate mucoid material stand out as round holes in the sections, giving the ' adenoid cystic ' appearance of some authors (Fig. 290). The density of closely packed cellular tissue, and the amount of the supporting stroma, vary very much and

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A D E N O M A T O U S T U M O U R S O F A N T E R I O R F O R E G U T 251

had seen about twenty cases in various sites. He used the term cylindroma to describe the histology of one of these, and, from his descriptions, others were undoubtedly mixed adenomas. He gave details of one case, a tumour of the cheek, which had been

may lead to difficulty in distinguishing cylindromas from mixed adenomas in small biopsies. Mitoses are not at all numerous. Fig. 296 stained by the periodic-acid Schiff method, shows the successive zones or cylinders which were the source of the

FIG. z93.-Cylindroma donum of back of tongue. Two years’ history. Excised and treated by irradiation. Re- operation a year later. Died four years after the initial treatment with local necrosis and dmical metastases in glands and lungs.

descriptive term ‘cylindroma’. Thus, there is a central blob of mucous surrounded successively by a hyaline ring, a ring of cells, another hyaline ring, and finally the fibrous stroma which also assumes a cylindrical or tubular shape. These details are seen especially in the oldest parts of the tumours.

When the mucous glands surrounding the tumour are available for examination it is possible to trace the origin of the neoplasia to the mucous gland ducts. Fig. 293 is a low magnification of the back of the tongue, in which healthy mucous glands are seen lying loosely between muscle bundles. The tumour is embedded in the same way and is seldom encapsulated as are the mixed tumours of the large serous salivary glands.

The mixed adenomas from which the cylindromas have to be distinguished show a variety of patterns which depend upon a curious process of auto- digestion in which areas of mucoid material emerge, and in which cartilaginoid and myxomatous metaplasia may develop. The epithelial cells scattered about in this mucoid or fibro-mucoid matrix appear to lose their polarity. This inextricable interming- ling of mesenchymal and epithelial elements under- going degenerative changes has been responsible for the great confusion in the histological descriptions of mixed adenomas, both before and since modem fixation and staining methods became available.

HISTORICAL SURVEY The history of the pathology of the foregut

adenomas is one of the particularly confused chapters of medical investigation, the beginnings of which did not forecast the ultimate confusion, for in 1859 Billroth described salivary adenomas, of which he

FIG. z94.-Higher magnification of Fig. 293 to show the relation of the tumour to mucous glands and its apparent origin from their ducts.

FIG: ,z95.-Tumour of antrum and palate treated by surgical excision. No recurrence recognized in four years. ( x so.)

followed for 23 years, and which was operated upon nine times and finally remained untreatable.

After that time cases were published under different names, and for years much discussion ensued as to whether the cells in these tumours were epithelial or endothelial in origin. Boettcher (1867,


1868) called them ‘ schlauchknorpel geschwiilst parotid mixed tumours, and he accepted their cylindrome ’, which to-day would mean that they heterogeneous appearance as supporting Conheim’s were both mixed tumours and cylindromas. theory of tumour genesis. He classed thirty-one Koestler (1867) described ‘ cancroids ’ which he cases as adenomas, none of which, although of many decided were the same as Billroth’s cylindromas : one years’ duration, showed any metastases. Wood, i n

FIG. z96.-Cylindroma of palate stained by the periodic-acid Schiff method to show the details of the pattern.

FIG. 197.-Metastasis in ilium from cylindroma in ptcrygo- mandibular region. History of deafness for ten years, now ear discharge and swelling of the face and neck on the same side. Removal of neck glands a year later and local recurrence recognized and also this bone deposit. ( x 30.)

Treated by X rays.

FIG. 298. - Silent metastasis in lung from a cylindroma in the region of the tonsil. History.

of his cases was in the sublingual region, and the other at the angle of the eye. In 1872 Waldeyer recognized that parotid tumours were the most ‘ mixed ’ of all tumours, and compared them with mixed tumours in other organs. By 1883 Malassez was able to collect eleven synonyms for what he accepted as a cylindroma, but preferred to call them ‘ epitheliomes alveolaires avec evahissement myxo- mateux ’. He added two cases of his own, one from the palate, and one from the submaxillary region.

In a study of tumours of the palate, Stephen Paget (1886) recognized that many of them were like

1904, wrote a long discussion on mixed tumours of the salivary glands. He had seen forty-seven cases in various sites, and used the term cylindroma for one, but attached no prognostic significance to it. Ribbert gave an authoritative ruling on what the word cylindroma meant in 1907, indicating that the cylindromatous tissue layers involved both the epithelial structures and the supporting stroma (Figs. 295, 296). He believed that they arose in the ducts of mucous glands and quoted one case where the tumour had spread slowly from the palate to the base of the skull, and had finally metastasized to the lungs. Krompecher (1908) reviewed the whole subject about the same time, under the heading ‘Bazalzellen Krebs ’, in which he included both cylindromas of mucous membranes and basal cell skin tumours.

From about this date readers find it increasingly easy to understand what histological pattern is involved in descriptive papers because of the great improvement in methods of illustration. Blumenfeld (1914) published the description of two heterotopic mixed tumours of the lip, one of which appears to have been a mixed adenoma, and the other a cylindroma. Patey in 1930 made a histological study of fifty-five salivary gland mixed tumours and noted the confused terminology : no follow-up data were included in his paper. I n the same year Brunschwig described and illustrated two cylindromas, from the tongue and sublingual regions, of seven and seven- teen years’ duration respectively. Spies (1930)

A D E N O M A T O U S T U M O U R S

followed twenty-nine cases of what he called cutaneous and non-cutaneous adenoid cystic carcinomas, three of which developed metastases, and the illustration of one of these is undoubtedly a cylindroma. He found the non-cutaneous group of these adenoid cystic tumours had a very much worse prognosis than the cutaneous group. New and Childrey (1931), in surveying tumours of the tonsil and pharynx, wrote of adenocarcinomas of mixed type which did not recur or metastazise. Lerow and Leroux (1934) subdivided the salivary gland turnours into fourteen varieties. In Ahlbom’s monograph (1935) on mucous and salivary gland tumours, cylindromas were classed among the semi- malignant tumours, and he called them ‘ basaliomas ’. Lemlitre, Andoin, and Lemlitre (1936) took up the word cylindroma again in the study of ectopic adenomatous tumours found in the skin and mucous membranes of the head region, and thought d’aspect cylindromateux might be applied to them and that cylindroma should be given up.

It was about this time that adenomas of the bronchus became widely recognized, and in a paper by Jackson and Konzelmann (1937) twelve cases were described. One of the illustrations is a cylindroma. In 1938 Harvey, Dawson, and Innes reviewed a large collection of mixed tumours of the salivary glands and decided that it was wisest to class them all as adenomas. There was no follow-up record of cases in this review, and those of the cylindroma pattern were not given any prognostic connotation.

Ringertz (1938) in the monograph on the malignant tumours arising in the nasal and para-nasal sinuses employed the word ‘ basalioma ’ as Ahlbom had done, and divided them into cystic and solid: his illustrations are those of the cylindroma pattern. In 1939 Kramer described six cases of cylindroma of the upper air passages, and Foster-Carter (1941) summarized the literature on bronchial adenomas to date, adding twenty-two of his own. He noted that they occurred most frequently in women, and it appears from his illustrations that adenomas of the cylindroma pattern were in his series.

Mulligan (1943) collected data of metastases from mixed tumours, and said that the cylindroma pattern was correlated with the tendency to metastasize. His own case was a tumour of the parotid of thirteen years’ duration, which eventually metastasized to bone and internal organs.

Tinney’s review (1945) of the tracheal tumours seen in the Mayo clinic over ten years included eight cylindromas, and all had a relatively good prognosis.

McDonald, Moersch, and Tinney (1945) saw forty-four adenomatous tumours of the bronchus, of which six were classed as cylindromas.

Quattlebaum (1946) discussed what he called adenocarcinomas of cylindroma type in the parotid gland, and indicated that the pathologist could be of real help to the surgeon by recognizing its specific pattern because of its tendency to recurrence and metastases. Of 20 cases only 5 were alive and well after five years, and 4 others had a history of prolonged recurrences ; the others were dead.

McDonald and Havens (1948) studied a large number of glandular neoplasms of the lips, nasal, and para-nasal cavities, and emphasized that the five-year survival rate of the cylindromas was better than that

O F A N T E R I O R F O R E G U T 253

of the adenocarcinomas, but that their ultimate prognosis was worse.

Belsey and Valentine (1951) described the histology of three cylindromatous mucous gland tumours of the trachea and bronchi, and, discussing their similarity to salivary gland tumours and basal cell skin cancers, emphasized their local invasive tendencies, although they rarely metastisized. They suggested that cylindromas should be classified as a special subgroup of the mucous gland tumours of the trachea and bronchi.

Pollack (1952) described two slowly growing cylindromas as ‘ relentlessly recurring ’ tumours ; one was in the nasopharynx, and the other in the antrum. This epithet, ‘ relentless recurrence ’ sums up the clinical course of the tumour very ably.

In Foote and Frazell’s study (1953) of over 500 tumours of the major salivary glands 34 of the adenoid cystic carcinoma type are included, and they were cylindromas as judged by the pictures.

These references are a selection from many papers which indicate that some workers have recognized a clinical entity among the adenomatous tumours of the anterior foregut region, and this is especially true of the oto-laryngological units within the last twenty years. Cylindroma appears to be the name under which it is most commonly described. The surgical pathologist can give substantial assistame to the surgeon by recognizing its pattern, because it is correlated with insidious infiltrative growth and grave ultimate prognosis.

DISCUSSION It has never been easy to assess the malignancy

of the relatively well differentiated adenomatous tumours. Over a hundred years ago the problem emerged in the study of breast neoplasms, and as soon as cellular pathology was established the adenomatous tumours of other organs, especially those of the skin, thyroid, ovary, and salivary glands, illustrated the same difficulties.

To-day the difficulties remain, and for various reasons. One of them is the comparative rarity of -adenomas : one worker may not see more than half a dozen cases from one site in a lifetime’s work. Further, without the support of a clinical follow-up record system, it is impossible to correlate a histological pattern with ultimate prognosis and survival time. A third factor which adds to diagnostic difficulties is the inadequacy of biopsy material which may be too small to include the relations of a tumour to its surroundings, or be distorted by sepsis and previous treatment. The scattering of histology material throughout the laboratories of different surgical units also prevents any wide view of tumour pathology being established. However, in radio- therapeutic centres it is still possible to investigate a wide range of material from the sites of the ‘ accessible cancers ’ at least. It is from a survey of ten years’ collection of specimens from accessible cancers that the cylindroma has emerged from among the mixed and other adenomatous tumours as a histological and clinical entity. It is also clear from the literature of the last fifteen to twenty years that some workers, in oto-laryngological units particularly, have increasingly recognized the importance of identifying this tumour on account of its grave


prognosis. I t is not clear, however, from the literature, that surgeons and pathologists as a whole have realized the prognostic importance of its histological characters.

Whether this neoplasm is essentially of mucous gland rather than of serous salivary gland origin is difficult to say, but it seems likely that anatomical and physiological differences may account for its clinical and histological peculiarities.

The serous salivary gland tissue of the anterior foregut region is concentrated in the parotid and submaxillary regions where the mixed adenomas are commonly found; and although there are also serous elements in the vallate papilk of the tongue and in the sublingual region, the main glands of the mucous membranes of the oral, nasal, and para- nasal cavities are of the mucous type. And we have shown that it is in the buccal and nasal cavities that the cylindromas are usually situated.

I t is noteworthy that adenomas of both mixed and cylindroma pattern are commoner in women than in men, the proportion being about 3 : 2.

SUMlMARY A survey of ten years' collection of adenomatous

and mixed adenomatous tumours of the anterior foregut region showed that those of the cylindroma pattern bear a worse prognosis than those of the ordinary mixed adenoma types. The cylindromas appear to arise in mucous rather than in serous salivary gland tissue, and are commonest in the ectopic, or aberrant sites. They have been obtained from the lacrimal gland and from the whole respira- tory tract, from lips and nose to the bronchi.

Their grave prognosis does not depend upon inaccessibility, but rather upon the fact that frequently they are not well encapsulated as are the adenomas in the large serous gland sites.

The mode of spread of a cylindroma is that of a relentlessly recurring rodent turnour and invasion of the base of the skull may occur before distant metastases arise. A few such distant metastases are illustrated.

It is suggested that the name cylindroma be accepted for this tumour, as it is now correlated with a special clinical picture and prognosis. No advantage can accrue from classifying it among the frank carcinomas which run a different morbid anatomical and clinical course.

The surgical pathologist substantially aids the surgeon by recognizing it because the general consensus of surgical opinion in the literature emphasizes the need for early radical excision. There is no evidence that it is a radio-sensitive lesion.

I have to thank Professor Victor Lambert and Mr. Kenneth Harrison for close co-operation in this

review, the latter supplied me with the clinical data of the cases. T o Dr. E. K. Dawson I am indebted for permission to study the bronchial adenomas in the histology collection of the Royal College of Physicians Laboratory in Edinburgh, and also for giving me Figs. 290 and 292 from that collection.

T o Mr. E. J. Higgins I am grateful for many histological preparations, and to Mr. F. Wardlaw for the photographs.

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I, 123, 186.

35, 357.

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201.

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Adenomatous tumours of the anterior foregut region showing the cylindroma pattern