Mucinouscystadenoma and cystadenocarcinoma the mucoceleand · is caused by dissemination of a mucinous cystadenocarcinoma within the peritoneal cavity. The special problems ofhistological

J. clin. Path., 1973, 26, 413-421

Mucinous cystadenoma and cystadenocarcinomaof the vermiform appendix with particularreference to mucocele and pseudomyxomaperitoneiN. M. GIBBS

From the Area Laboratory, St Luke's Hospital, Guildford, and the Research Department,St Mark's Hospital, Londont

SYNOPSIS Ten cases of mucocele of the vermiform appendix are described. Eight cases were ofmucinous cystadenoma of the appendix and six cases showed acute inflammation. Two of the sixcases showed pseudoinvasion of the appendix and in a further case the appendix had perforatedwith extrusion of a misplaced neoplasm. Two cases were of mucinous cystadenocarcinoma and oneof these was diagnosed as 'pseudomyxoma peritonei'. 'Pseudomyxoma peritonei' is a misnomer andis caused by dissemination of a mucinous cystadenocarcinoma within the peritoneal cavity. Thespecial problems of histological diagnosis are discussed.

Mucocele of the appendix is an uncommon butmysterious condition about which a large volume ofliterature has accumulated without much clarifica-tion of the underlying pathology. There are two maintheories of causation. The first can be termed the'obstructive' theory because it is thought that thedistal mucosa of the appendix is stimulated toproduce an excessive secretion of mucin, as a resultof proximal obstruction of the lumen by faeces,inflammatory fibrosis, or the presence of a neoplasm(Elliott, 1957). The second theory, which is anextension of the first, asserts that the mucosa of theobstructed appendix undergoes an ill definedneoplastic change which has been termed 'adeno-carcinoma grade I' (Woodruff and McDonald,1940) or papillary mucus-secreting carcinoma in situ(Scimeca and Dockerty, 1955).The mystery deepens when 'pseudomyxoma

peritonei', which is a complication of mucocele ofthe appendix, is considered. The original hypothesis(Werth, 1884) postulates that peritoneal irritation,produced by the leakage of mucus from a burstmucocele, causes a metaplastic reaction to takeplace in the mesothelial cells so that mucin is formedlocally in the peritoneal cavity. Other hypothesesaccept that malignant adenocarcinomas of theappendix can produce pseudomyxoma peritonei, butthere is also the opinion that it may occur in theReceived for publication 5 April 1973.

presence of a neoplasm which is not invasive orwhere there is an abnormal epithelium which is notneoplastic.The object of this paper is to describe the histology

of 10 appendices and to consider the underlyingpathology with particular relation to mucocele andpseudomyxoma peritonei.

Materials and Methods

The appendices were fixed in 10% formal saline.Coronal blocks in sequence were taken so that theentire appendix was examined in each case with theexception of cases 3, 6, and 10. Sections were cut at5,u and stained routinely by Ehrlich's acid haema-toxylin and counterstained with eosin. Specialstains included phloxine tartrazine for Paneth cells,the diazo method, and Fontana's silver impregna-tion for enterochromaffin granules, alcian blue, andPAS (pH 2 6) for mucin.The cases are summarized in table I.

Histology

The histological details of cases 1-10 are given intable II.

Cases 1-8 showed a replacement of the liningepithelium of the surface and the glands by tallcolumnar mucinous epithelium which characteris-413

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Case No. Date Sex Age in Clinical History Follow UpYears

1 March 1972 76 Incidental finding at necropsy for basilar arterialthrombosis

2 March 1971 V 59 Presented with acute abdominal pain, and laparotomy Complete recoveryrevealed perforated diverticulum of the caecum and amucocele of the appendix. The appendix was removed.

3 November 1957 54 Presented with acute abdominal pain and Complete recoveryappendicectomy was done followed by an intervalright hemicolectomy.

4 June 1972 47 Acute abdominal pain followed by appendix mass for Complete recoverysix weeks, and appendicectomy

5 September 1972 37 Acute appendicitis and appendix mass followed by Complete recovery'interval' appendicectomy three months later

6 January 1957 70 Acute appendicitis associated with localized abscess Alive and well whenfilled with mucoid pus last seen in 1963

7 March 1972 70 Acute appendicitis and appendicectomy Complete recovery8 October 1972 71 Abdominal pain followed by a mass in the abdomen Complete recovery

for four months; this was explored and an inflamedperforated distended appendix was removed.

9 June 1965 54 Two-day history of abdominal pain and distension; Complete recoveryan appendicectomy was done. A right hemicolectomywas done six weeks later

10 May 1971 d 45 There was abdominal pain and swelling for two Disseminated intra-months; an abscess in the lower abdomen was inabdominal adeno-cised and drained in May 1971. This recurred and much carcinomamucus was evacuated. A diagnosis of pseudomyxomaperitonei was made and a right hemicolectomy wasdone. Further accumulation of mucin occurred anda metastasis in the abdominal wall was biopsied inJune 1972.

Table I Clinical details of cases I to 10

tically showed basal crowding of nuclei and thepresence of numerous mitoses. The epitheliumlooked neoplastic, and villous processes weredeveloped in some cases (cases 4 and 5) with anappearance identical to the villous adenomas of thelarge intestine. In addition the glands were tortuousand showed lateral branching and budding of cystictubules (figs 1, 2, and 3). There were numerousmitoses and the basi-glandular cells of the cryptstended to be displaced by mucinous epithelium. Thusthe Paneth cells disappeared and argentaffin cellswere diminished and displaced, a common factor inneoplasms of the intestine which distinguishes themfrom hyperplasias and heterotopias (Gibbs, 1967).Polypoid mucosal hyperplasia (metaplasia) mayoccur in the appendix (MacGillivray, 1972) but theepithelium, although tall, only shows occasionalgoblet cells whilst the surface epithelial cells have aveiled or fronded appearance.

Cases 1 and 2 showed 'sac-like' dilatations(mucoceles) and here there was widespread pressureatrophy of the lining epithelium (fig 4) and partialreplacement by granulation tissue with a 'foreign-body' giant cell reaction. The glands were stretchedby accumulated mucin and many had disappeared.Nevertheless the characteristic neoplastic epitheliumwas preserved in occasional cul de sacs. It would seem

that further development of the tumours wasimpeded by mucus retention.

Cases 1, 2, 4, and 5 showed partial or completeorganic obstruction of the proximal lumen byfibrous tissue which had replaced or constricted theepithelial lining. It is possible that obstruction wasdue to congenital absence of part of the mucosa orpossibly to an episode of localized proximal inflam-mation. It seems more likely, however, that the viscidmucin secreted by the tumour was unable to draininto the caecum so that the adjacent normal mucosaunderwent pressure atrophy. The thickened tumourmucosa may have blocked the proximal lumen but ineither event the normal mucosa will be subject tocompression and inflammation with eventual atrophyand reactive fibrosis as sequelae. Alternativelyblockage could result from calcified inspissatedmucus (case 5, fig 5). It seems that if free drainage ofmucin from the tumour were possible a saculardilatation (mucocele) of the appendix would notdevelop.

Cases 3, 4, and 5 did not show diffuse dilatation ofthe appendices but instead developed diverticulaThese diverticula bulged through and betweenthe muscle coats and formed lakes of mucus lined inpart by mucinous epithelium. Acute inflammationhad occurred with consequent perforation and

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415Mucinous cystadenoma and cystadenocarcinoma of the vermiform appendix

Case Macroscopic Lumen Microscopic Description Appendix Other InformationNo. Description Diverticulum

I Appendix (6 x 2 Proximal half of The distal mucosa was replaced bycm) showed gross lumen showed columnar mucinous epithelium which wasdistension of distal fibrous obliteration. stretched and flattened. Most of the cryptshalf by mucus. had disappeared.

2 Appendix (6 x 1-5 Proximal lumen The distal mucosa was replaced by tallcm) showed gross showed fibrous columnar mucinous epithelium. The glanddistension of distal obliteration. crypts had disappeared.part by mucus.

3 Appendix showed The mucosa of the dilated part wasdistension of the replaced by tall columnar mucinousmiddle part by epithelium which showed areas of flatteningmucin and pus. and inflammation.

4 Appendix (4 x 0-8 Proximal lumen The distal mucosa was replaced by tallcm) showed distal showed fibrous columnar mucinous epithelium showingdilatation (1-5 x I obliteration. branched papillary processes, but foci ofcm) and globules atrophy and inflammation were present.of mucin could beseen beneath theperitoneal coat.

5 Appendix (5 x 2 Proximal lumen The distal mucosa was replaced by tallcm) showed distal obliterated by mucinous columnar epithelium whichdilatation and was fibrous tissue; formed papillary processes projecting intofilled with mucin distal lumen the lumen. The glands were elongated andand pus. There was contained a showed pronounced lateral branching andan old perforation calculus mitotic activity.with adhesion to thecaecum and adeposit of jelly-likemucin.

6 Appendix was The distal mucosa was replaced bydistended with pus disrupted tall columnar mucinous epitheliunand mucus and There was diffuse acute purulentthere was a perfora- inflammation.tion and abscess.

7 Appendix distended Acute purulent inflammation of theby pus and mucin; appendix; crypts were replaced by atypicaladherent to caecum tall columnar mucinous epithelium whichwhich showed showed a surface villous pattern andgangrenous necrosis. tortuous glands.

8 Appendix was There was marked inflammatory thickeningdistended with pus and the mucosa was replaced by talland mucus and was mucinous columnar epithelium. There wereperforated. surface villous processes and hyperplastic

9 Appendix (6 x 3 Patentcm) was sealed withomentum and hadnot perforated.The distal three-quarters of theappendixwere distended bymucin and the wallwas thickened.

10 Appendix wasfragmented andinvolved by atumour mass and anabscess.

glands although in places the epitheliumwas stretched and attenuated.The proximal glands were normal but theremainder were hyperplastic and replacedby tall columnar mucin-secretingepithelium. The distal half was infiltratedby mucinous adenocarcinoma showing alarge glandular pattern; 'signet-ring' cellswere present; numerous argentaffincells in both large tubules and 'signet-ring'cells.

There was a primary mucinousadenocarcinoma of the appendix with acomplex acinar pattern, and surrounded by'lakes' of mucin. Argentaffin cells were notseen.

Absent

Absent

Present No residual growthfound in caecum andascending colon

Present

Rupture of diverti-culum into theinterstitial tissues ofthe appendix and'displacement' offragmented mucosa

No extension ofgrowth into caecum;lymph glands inappendix mesenterydid not containmetastases.

m.

Absent

Epithelium was dis-placed into the musclecoats at the site ofperforation but nodiverticulum.

Absent An interval righthemicolectomy wasdone and the ileo-caecal lymph glandscontained metastases.

Diffuse invasion ofthe peritoneum; nodiverticulum

Interval right hemi-colectomy showedcarcinoma of theappendix invading thecaecum; developedmetastases inabdominal wall.

Table II Histology ofappendices

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8'23% by tall mucinous epithelium (haematoxylin and eosinx 80).Fig 3 Case 3: inflamed mucocele showing distorted

i villous epithelium (haematoxylin and eosin x 63).

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showing villous processes and calcified secretion(calculus) (haematoxylin and eosin x 63).

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Fig 7 Case 5: epithelial displacement andpseudoinvasion in a perforated mucocele ofappendix(haematoxylin and eosin x 100).

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Mucinous cystadenoma and cystadenocarcinoma of the vermiform appendix

Fig 11 Fig 12Fig 11 Case 9: mucinous cystadenocarcinoma of appendix showing numerous argentaffin cells (Fontana's sill ercounterstained with saffranin, x 100).Fig 12 Case 10: mucinous cystadenocarcinoma of appendix with abdominal metastasis (haematoxylin and cosinx 63).

disruption of the lining epithelium. Strips of displacedepithelium could be seen lying interstitially producinga semblance of invasion (figs 6 and 7) and mucinousepithelium had grown through the perforationtracks in cases 4 and 5. Large numbers of macro-phages were present in the interstitial mucin and thiscomplicated the histology (fig 8).

Cases 1-8 cover the histological 'spectrum' of anepithelial neoplasm of the appendix which isconsidered to be a primary mucinous cystadenoma.It can be seen that considerable variations in his-tology occur in these neoplasms which appear to bethe result of local factors influencing tumourgrowth.Case 9 was an invasive mucinous neoplasm of the

appendix forming large numbers of argentaffin cellsand was considered to be a primary mucinous cysta-denocarcinoma of the appendix (figs 9, 10, and 11).

There was acute appendicitis wihout perforation sothat peritoneal dissemination had not occurredalthough there were lymphatic metastases. Case 10was a similar tumour but perforation and appendixabscess had occurred which was followed by dis-se;mination of the mucinous cystadenocarcinomawithin the peritoneal cavity and 'pseudomyxomaperitonei' (fig 12).

Discussion

Mucinous cystadenoma of the appendix is anuncommon tumour which secretes viscid mucus thattends to accumulate within the lumen so that itbecomes distended to produce a mucocele. If thelumen proximal to the tumour is narrow, the mucusmay not drain. However, four of the mucocelesdescribed here are associated with severe narrowing

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N. M. Gibbs

or complete obstruction of their lumina which isprobably related to abnormalities in development ofthe organ or subclinical episodes of acute inflam-mation. It is evident that epithelial displacement andpseudoinvasion are related to definite clinicalepisodes of acute appendicitis. In longstanding casescalcification of inspissated mucus (case 5) may resultin the formation of an appendiceal calculus (Bunch,1945) which may be detected radiographically(Marshak and Gerson, 1960).Mucinous cystadenoma of the intestine is found,

it seems, only in the appendix. However, it sharesmany of the morphological characteristics of villousadenoma of the colon and it can be argued that thetumours described are in fact villous adenomas whichhave been altered by the confines of the appendix.Nevertheless it is known that epithelial neoplasms ofthe appendix show significant differences fromneoplasms elsewhere in the intestine. For example,the appendix is the most common site of carcinoidtumours which, in this situation, are almost alwaysbenign, often show mucin secretion, and may con-tain Paneth cells. Furthermore some primaryadenocarcinomas of the appendix show histologicalfeatures not found in other organs.The cases of mucocele described in this paper show

the characteristic epithelial abnormalities common toreports in the literature when a detailed examinationof the appendix has been made. The nature of theabnormalities, however, has been fogged by muchdubious and imprecise terminology. Many authorshave been unable to decide whether the epitheliallesion is metaplastic or neoplastic, benign ormalignant, and others diagnose carcinoma in situ,which is a concept best avoided in the considerationof neoplasms of the intestine. The reasons for theapparent contradictions seem to depend on specialproblems of interpretation. The neoplastic epitheliumforming the mucocele may undergo deformation dueto pressure of accumulated mucus so that theepithelium may become flattened or atrophic. Thusthe neoplastic epithelium of the mucocele may passunrecognized unless a detailed histological examina-tion of the appendix is undertaken. Furthermore, theneoplastic cells of the mucocele, whether invasive ornot, usually do not show cytological proof ofmalignancy, a finding in common with otherneoplasms of the intestinal tract. The presence oflarge pools of mucin may distort local anatomy andwhen perforation takes place the epithelium may bedisplaced and extruded into the peritoneal cavitysimulating invasion. A similar problem of inter-pretation is encountered in adenomatous polyps ofthe colon, which may show displacement of glan-dular tissue into the stalk. This displacement may bemistaken for malignant transformation and invasion.

It can be seen, therefore, that a distinction betweenbenign and malignant mucinous cystadenoma maybe a difficult problem. This provides an explanationfor the observation made by Hilsabeck, Judd, andWoolner (1951) that the majority of cases diagnosedhistologically as malignant failed to progress oncethe mucocele was removed and that only two of 18patients with mucocele developed pseudomyxomaperitonei and died. The clinical diagnosis may alsobe problematic as a very large pseudocyst filled withmucin may form around a perforated mucocelewhich may be mistaken for 'pseudomyxoma peri-tonei' (Early, Stephenson, and Davis, 1968).However, the problem of interpretation is simplifiedif the histologist is aware of the possibility ofpseudoinvasion by displaced islands of neoplasticepithelium in an area of inflammation. Conclusiveevidence of tissue invasion must be found before adiagnosis of mucinous cystadenocarcinoma is madeand this was readily available in the examplesdescribed (cases 9 and 10). Benign mucinouscystadenomas (mucoceles) should be treated byappendicectomy and more radical procedures areunnecessary.Mucinous cystadenocarcinoma behaves as an

invasive neoplasm (cases 9 and 10). Such tumours,in common with other mucinous adenocarcinomasof the intestinal tract, may produce by differentiationlarge numbers of argentaffin cells and have beenmistaken for carcinoids (Evans and Murphy, 1959).A tumour which invades and disseminates within theperitoneal cavity after the appendix has been totallyremoved must be regarded by definition as malig-nant.The alarming clinical features produced by dis-

semination of a mucinous carcinoma within theperitoneal cavity were described by Fraenkel (1901)in relation to mucocele of the appendix. He used theterm 'pseudomyxoma peritonei', which had originallybeen given by Werth (1884) to describe a similarclinical picture associated with 'cystadenoma' ofthe ovary. Certainly pseudomyxoma peritonei is amisnomer with emotive connotations which eventoday causes histologists and clinicians to cast asiderecognized precepts of disease. It should be leftbehind with the past.

I wish to thank Dr B. C. Morson and the surgeonsof St Luke's Hospital, Guildford, St Peter's Hospital,Chertsey, and St Mark's Hospital, London, forpermission to study their patients, and Dr G. F. Rossfor pathological material of two cases.References

Bunch, G. H. (1945). Mucoid disease of the appendix. Ann. Surg., 121.704-709.

Earls, K. S., Stephenson, D. V., Jr., and Davis, W. C. (1968). Giant

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Mucinous cystadenoma and cystadenocarcinoma of the vermiform appendix

retroperitoneal mucocele simulating pseudomyxoma peritoneiand mucinous adenocarcinoma. Amer. J. Surg., 116, 439-443.

Elliott, C. E. (1957). Two cases of pseudomyxoma peritonei frommucocele of the appendix. Brit. J. Surg., 45, 15-18.

Evans, R. W., and Murphy, A. F. (1959). Pseudomyxoma peritoneiassociated with an appendix obstructed by an argentaffinoma(carcinoid) in a male. Brit. J. Surg., 47, 166-172.

Fraenkel, E. (1901). Uber das sogenannte pseudomyxoma peritonei.Munch. med. Wschr., 48, 965-970.

Gibbs, N. M. (1967). Incidence and significance of argentaffin andPaneth cells in some tumours of the large intestine. J. clin.Path., 20, 826-831.

Hilsabeck, J. R., Judd, E. S., Jr., and Woolner, L. B. (1951). Sym-posium on surgical aspects ofcancer problem: carcinoma of the

vermiform appendix. Surg. Clin. N. Amer., 31, 995-1011.MacGillivray, J. B. (1972). Mucosal metaplasia in the appendix. J.

clin. Path., 25, 809-81 1.Marshak, R. H., and Gerson, A. (1960). Mucocele of the appendix.

Amer. J. dig. Dis., 5, 49-54.Scimeca, W. B., and Dockerty, M. B. (1955). Carcinoma of the vermi-

form appendix: a review of the literature and report of a case.Proc. Mayo Clin., 30, 527-534.

Werth, R. (1884). Klinische und anatomische Untersuchungen zurLehre von den Bauchgeschwiilsten und der Laparotomie. Arch.Gynik., 24, 1)0-118.

Woodruff, R., and McDonald, J. R. (1940). Benign and malignantcystic tumors of the appendix. Surg. Gynec. Obstet., 71, 750-755.

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Mucinouscystadenoma and cystadenocarcinoma the mucoceleand · is caused by dissemination of a mucinous cystadenocarcinoma within the peritoneal cavity. The special problems ofhistological