Malignant fibrous of salivary glands - From BMJ and ACP · malignant fibrous histiocytoma arising in salivary glands are presented andthe features ofseven previouslyreportedcasesare

J Clin Pathol 1982;35:946-953

Malignant fibrous histiocytomas of salivary glandsE BENJAMIN, S WELLS, H FOX, NL REEVE, F KNOX

From the Departments of Pathology, University of Manchester, Manchester M13 9PT, and Stepping HillHospital, Stockport, Cheshire

SUMMARY The light microscopic, immunohistological and ultrastructural findings in two cases ofmalignant fibrous histiocytoma arising in salivary glands are presented and the features of sevenpreviously reported cases are reviewed. This neoplasm is extremely rare in this site and may poseproblems in diagnosis. It has to be distinguished from other spindled cell tumours, in particularfrom epithelial tumours of predominantly spindled cell pattern; immunohistological markers forhistiocytic cells may be of value. The histogenesis of this neoplasm is controversial but our

electron microscopic findings support an origin from mesenchymal cells which differentiate alonga broad fibrohistiocytic spectrum.

Mesenchymal tumours of the salivary glands arerare and constitute < 5% of all primary salivarygland neoplasms in adults.' Lipomas, haeman-giomas, lymphangiomas, neurofibromas andneurilemmomas form the bulk of these uncommonsalivary gland tumours and malignant mesenchymalneoplasms of the salivary glands are of extreme rar-ity.We report here two recently encountered exam-

ples of malignant fibrous histiocytoma arising insalivary glands, one occurring in the parotid glandand the other involving the submandibular gland.

Material and methods

Formalin-fixed, paraffin-embedded sections ofbiopsy material were stained with haematoxylin andeosin, Masson's trichrome, reticulin, Perls' stain,elastic van Gieson, periodic acid-Schiff (PAS), PASafter diastase digestion and phosphotungstic acidhaematoxylin.

Staining for lysozyme (muramidase), alpha-i-antitrypsin (a,AT) and alpha-i-antichymotrypsin(a,ACT), used as histiocytic markers, was per-formed using the immunoperoxidase (PAP) techni-que.2 All antisera were obtained from Dako (MerciaBrocades, Surrey) and appropriate positive andnegative controls were incorporated. Four randomlyselected cases of fibrous histiocytoma occurring inother locations and four spindled cell variants ofmixed salivary adenoma were also studied for thesemarkers.

Tissue for electron microscopy had to be retrieved

Accepted for publication 7 January 1982

from paraffin-embedded blocks in both cases.Selected areas were dewaxed, post-fixed in osmiumtetroxide and processed by standard methods.Ultrathin sections were stained with uranyl acetateand lead citrate and viewed with a Philips EM 301electron microscope.

Case reports

CASE 1A 28-year-old woman presented in May 1981 with aswelling in the left preauricular region of six months'duration. It had been an incidental finding on selfpalpation and there were no related symptoms.Examination revealed a poorly defined swelling 1-0cm in diameter in the region of the left parotidgland. It was deeply fixed with no skin tethering andwas not tender. The remainder of the physicalexamination was normal as were results of routineinvestigations.A presumptive diagnosis of mixed salivary

adenoma was made and exploration of the parotidgland and superficial parotidectomy carried out. Asmall branch of the facial nerve was found entrap-ped within the tumour and had to be sacrificed.Postoperatively she developed left sided facial para-esthesia and ptosis due to weakness of theorbicularis oculi: this however improved within afew days. At follow-up five months later there wasno recurrence or lymphadenopathy.

PathologyThe resected parotid lobe measured 2 x 2 x 1 cmand was partially replaced by firm, grey white tissue.

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Malignant fibrous histiocytomas of salivary glands

Microscopically a rim of normal parotid tissue sur-rounded a well defined but non-encapsulated spin-dled cell tumour. The spindled cells formed interlac-ing fascicles and whorls with a well markedstoriform pattern in many areas (Fig. 1). A variableamount of collagenous stroma was present, mostabundant at the periphery. Centrally the tumour wasmore cellular and the spindled cells much plumper.Scattered throughout the tumour, but predominantcentrally, were multinucleated tumour giant cellsoften with a Touton-like appearance (Fig. 2). Slit-like vascular spaces were prominent in the centralportion of the tumour and there was marked extra-vasation of red blood cells. Haemosiderin pigment,identified by iron stains, was abundant in this area.Mitotic figures were noted but the overall mitoticactivity was low. At its margins the tumourinfiltrated parotid tissue and there were focal lym-phoid aggregates. A few residual ducts were entrap-ped within the tumour in this area but multiple sec-tions did not reveal epithelial elements elsewhere inthe tumour.Immunoperoxidase studies showed granular

brown staining for lysozyme, a1AT and a1ACT intumour giant cells and in plump spindled cells in thecentral portion of the tumour. Spindled cells at theperiphery of the tumour were mostly negative.

Electron microscopyTissue preservation was not optimal for electronmicroscopy but several cell types could be identified.Fibroblast-like cells were the most numerous andpossessed indented nuclei and elongated cyto-plasmic extensions. They contained abundant roughendoplasmic reticulum (RER), often with dilated

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Fig. 1 Case 1: malignant fibroushistiocytoma ofparotid gland showing a wellmarked storiform pattern and entrapmentof residual ducts by tumour. Haematoxylinand eosin x so

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Fig. 3 Case 1: electron micrograph showing two fibroblast-like cells with irregular nuclei, elongated cytoplasmicextensions and abundant RER. Extravasated erythrocytes lie in the extracellular space. x 6250.

cisternae filled with floccular material but otherorganelles were scanty (Fig. 3). Another cell typepresent had moderate amounts of RER and manycompact bundles of myofilaments in their cytoplasm.Focal densities were present in some of thesemyofilament aggregates. Attachment plates werenoted along the cell margins and were often associ-ated with basal lamina-like material. These cellswere interpreted as myofibroblasts and cells showingmyogenic differentiation; typical smooth musclecells were however, not found. Histiocyte-like cellshad reniform nuclei and their cytoplasm contained afew cisternae of RER, free ribosomes, lysosomalbodies and empty fat vacuoles. Occasionally, cellsshowing features of both fibroblasts and histiocytes(fibrohistiocytes) were encountered. There werealso a number of small cells with smooth cell sur-faces, round nuclei and relatively clear cytoplasm inwhich organelles were very scanty (Fig. 4). Thesewere considered to be undifferentiated mesen-chymal cells. The extracellular space containedextravasated erythrocytes and collagen of normalperiodicity.

CASE 2A 65-year-old man with hepatosplenomegaly and awhite cell count of 166 x 106/l was diagnosed ashaving chronic lymphatic leukaemia (CLL) inMarch 1980. He was treated with prednisolone andcyclophosphamide and showed gradual clinicalimprovement. Four months later he presented witha swelling in the left submandibular region whichhad been rapidly enlarging over two months. He hadfirst noticed a swelling in that area two years previ-ously; it had decreased in size but apparently notcompletely disappeared with a course of antibiotics.His past medical history also included a basal cellcarcinoma of the nose, successfully treated byradiotherapy in 1979, and herpes zoster at the levelof D3, the same year.The submandibular swelling measured 5 cm in

diameter and was extremely tender. The clinicalimpression was of a leukaemic deposit or lym-phomatous transformation of CLL (Richter's syn-drome). On surgical exploration a tumour mass wasfound within the submandibular salivary gland andthe gland which was adherent to the mandible was

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Fig. 4 Case 1: an undifferentiated cell with round nucleus and clear cytoplasm containing scanty organelles. Afibroblast-like cell to the right contains floccular material within dilated RER. x 11 250.

excised. After surgery the mass recurred and he suf-fered considerable pain. A course of radiotherapysix weeks after the operation relieved the pain andproduced some diminution of tumour size. A monthlater the mass was enlarging again and measured 12x 10 cm; it now involved the left side of his face andalso extended across the midline below the chin.There was skin ulceration and ulceration into thefloor of the mouth. Antibiotics and chemotherapywith intravenous carminomycin produced littleimprovement. A chest x-ray at this time revealed anopacity considered to be a metastatic deposit in themidzone of the right lung. Terminally the tumourspread to involve the lips, mouth and right side of hisface. The patient died at home with no identifiableacute event in January 1981. A necropsy was notperformed.

PathologyThe excised submandibular salivary gland measured7 x 5 x 4 cm. On section there was loss of thenormal lobular pattern and replacement by greyhaemorrhagic tissue surrounding a central necroticand cystic area. Histologically a pleomorphic spin-dled cell tumour largely replaced the glandular

parenchyma. A storiform pattern was evident infocal areas and there were frequent multinucleatedtumour giant cells with abundant, eosinophilic cyto-plasm (Fig. 5). Mitotic figures, often abnormal, werenumerous. Small areas of necrosis were scatteredthroughout the tumour. At the periphery thetumour merged with residual ducts and acini ofsalivary gland tissue. A moderate degree of neutro-phil polymorphonuclear and lymphocytic infiltrationwas present thoughout the tumour. Trichrome stainsdemonstrated a variable production of collagenfibres.

Immunoperoxidase stains revealed coarse, browngranular staining for a,AT and a,ACT in both spin-dled and giant cells in several areas of the tumour(Fig. 6). With lysozyme finely granular staining wasseen in only a few cells in focal areas of the tumour.Neutrophil polymorphs present stained strongly forlysozyme and a,AT.

Electron microscopyUltrastructurally the tumour was composed of a var-iable cell population, as in case 1. Histiocyte-likecells were abundant and had irregular nuclei withlarge nucleoli and peripheral heterochromatin. The

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Fig. 5 Case 2: pleomorphic spindled and tumour giantcells and a diffuse inflammatory cell infiltrate. Haematoxylinand eosin x 160

Fig. 6 Case 2: (a) tumour cells showing coarse granularstaining for alACT. Immunoperoxidase x 350.(b) Granular cytoplasmic staining oftumour giant cells fora,AT. Immunoperoxidase x 350


cytoplasm contained numerous lysosomal bodies ofvarying size, fat vacuoles, laminated myelin figuresand coiled RER (Fig. 7). Their cell borders hadcomplex interdigitating processes. In occasional cellsthe cytoplasm was almost entirely filled by coales-cent fat vacuoles producing a "foamy" (xanthomat-ous) appearance (Fig. 8). Fibroblast-like cells hadlobulated nuclei, frequent nucleoli, abundant RERand a few fine cytoplasmic filaments. Undifferenti-ated cells similar to those in case 1 were also presentas were fibrohistiocytes of rather immature appear-ance having variable amounts of RER, free ribo-somes, lysosomal bodies and occasional cytoplasmicfilaments. Tumour giant cells possessed multiplenuclei with prominent nucleoli, abundant dilatedendoplasmic reticulum and a number of mitochon-dria.

Results of additional immunoperoxidase studies

The four fibrous histiocytomas studied (two sub-cutaneous malignant tumours, one malignantretroperitoneal tumour and one benign subcutane-ous tumour) all showed granular brown staining forlysozyme and a,AT in moderate to large numbers oftumour cells. Staining for a,ACT was negative inone subcutaneous malignant tumour and in thebenign fibrous histiocytoma but positive in the othertwo tumours.The spindled cells of all four spindled cell variants

of mixed salivary adenoma failed to stain the withlysozyme and a,AT. With a1ACT a variable numberof spindled cells were positive in all tumours. Typi-cal ductal structures, when present, stained posi-tively for a,ACT but less frequently for lysozymeand a1AT.

Discussion

Seven previous cases of fibrous histiocytoma involv-ing the salivary glands have been reported3-8 andthe main features of these, together with the twoexamples reported here, are summarised in theTable. Seven occurred in males and two in females,the ages of the patients ranging from 16 months to69 yr: the maximum incidence was in the 6th and7th decades. The time for which a mass had beenpresent before surgical exploration varied from 6 wkto 30 yr and the parotid gland was the more com-mon location than the submandibular gland (2:1).Four of these tumours were considered to bedefinitely malignant and three of these subsequentlyrecurred: two also metastasised to the lungs and onepatient (case 2 in our report) died at 5 months.

Case 2 of this report is of particular interest in thatthe patient had three malignant neoplasms diag-

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nosed over an 18-month period, a basal cell car-cinoma, chronic lymphatic leukaemia and a malig-nant fibrous histiocytoma. Weiss and Enzinger,9 intheir analysis of 200 cases of malignant fibrous his-tiocytoma, found that a second tumour occurred in13% of cases; most of these were carcinomas butone patient developed acute myeloid leukaemia. Itis also known that death from other malignant dis-ease is common in cases of chronic lymphaticleukaemia and that the incidence is higher than canbe accounted for by the predominance of elderlypatients and may in fact be related to immunodefi-ciency.'0 Lymphomatous transformation of chroniclymphatic leukaemia (Richter's syndrome), charac-terised by a pleomorphic lymphoid infiltrate withtumour giant cells, had to be distinguished frommalignant fibrous histiocytoma in this patient.

Considerable controversy surrounds the his-togenesis of fibrous histiocytoma. The original con-cept that this family of neoplasms was derived froma tissue histiocyte which has the capacity to evolveinto fibroblasts was based on histological and tissueculture studies." However, it is known that any tis-sue culture of mesenchymal cells can eventually

transform into a fibroblastic culture'2 andAlguacil-Garcia et al'3 contend that in vitro trans-formation between cell types do not prove theirorigin but merely that they can assume alternateforms under certain conditions.

Perhaps the most impressive evidence to date forthe histiocytic theory of origin of fibrous histio-cytomas is that of a transplantable tumour in micewith the characteristic morphological features. Thistumour has been shown to originate from peritonealmacrophages which have been thoroughly identifiedas histiocytes on the basis of histochemical,immunohistochemical, functional and ultrastruc-tural studies.'4An alternative theory of histogenesis is that the

neoplasm is derived from an undifferentiatedmesenchymal cell which differentiates along a broadfibroblastic and histiocytic spectrum reflected by col-lagen synthesis and, occasionally, phagocytosis. Sev-eral recent electron microscopic studies havedemonstrated in these tumours the presence offibroblast-like, histiocyte-like, fibrohistiocytic andundifferentiated cells'3 '5- and it has been post-ulated that the mesenchymal stem cell may pass

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Fig. 8 Case 2: part ofa xanthomatous cell in which the cytoplasm is filled by fat vacuoles. A centriole, some lysosomes anda few mitochondria are also present. An adjacent histiocyte-like cell contains numerous lysosomes. x 22 750

through a stage (fibrohistiocyte) in which features ofboth main cell types are present. I5 Our electron mic-roscopic findings in both cases of a population offibroblast-like, histiocyte-like, fibrohistiocytic andundifferentiated cells would support this theory,

although morphology alone would be insufficient toprove it. In addition, cells showing myogenic dif-ferentiation were present in case 1. Myofibroblastsand cells showing myogenous features have beendescribed in previous electron microscopic

Reported cases ofsalivary gland fibrous histiocytomas

Authorl Sex and Duration Location & size of Histological Initial Follow-upcase age (yr) of mass gland diagnosis treatment

O'Brien & M-69 ? 30 yr Submandibular Storiform Excision Well at 5 monthsStout (3) 4.5 x 3.5 x 2 cm fibrous xanthoma glandO'Brien & M-65 5 months Parotid Mixed fibrous Excision gland Well at 9 monthsStout (3) 3-2 x 2-2 x 1-7 cm xanthoma and neck nodesJunaid et al M-50 2 yr Right parotid Dermatofibrosarcoma Partial Recurrence at 6 yr with(4) 4.5 x 3.5 x 3 cm protruberans of parotidectomy skin infiltration

parotidBlitzer & M-54 Not known Right submandibular Malignant fibrous Excision gland Two recurrences and lungLawson (5) (size not known) histiocytoma metastasis in 2 yrNilsen & F-53 5 yr Right parotid Benign fibrous Superficial Well at 5 monthsLind (6) 2 x 2 cm xanthoma parotidectomyShapshay M-16 6 wk Right parotid Fibrous Total parotidectomy Not knownet al (7) months 3 x 3 cm histiocytomaFayemi & M-46 "many Left parotid Benign fibrous Superficial Well at 3 yrAli (8) months" 4 x 3.5 cm histiocytoma parotidectomyPresent F-28 6 months Left parotid Malignant fibrous Superficial Well at 5 monthscase 1 2 x 2 x 1 cm histiocytoma parotidectomyPresent M-65 2 yr Left submandibular Malignant fibrous Exision gland Post-op recurrence andcase 2 7 x 5 x 4 cm histiocytoma lung metastasis. Died with

disease at 5 months

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studies 13 11 and probably represent a variation inmesenchymal differentiation.Immunoperoxidase studies for lysozyme, ajAT

and a1ACT described as markers of histiocyticcells'9-2' showed positive staining cells in both cases.Staining was also consistently positive for lysozymeand a,AT in four randomly selected cases of fibroushistiocytoma but variable with a,ACT. Meister eta120 have studied a larger number of malignantfibrous histiocytomas using lysozyme and a,ACT.They found that staining for lysozyme was moreselective but less frequently found whilst a,ACr wasnot found in all cells which on routine stains werecompatible with histiocytes and was sometimes posi-tive in non-histiocytic tumours. In our opinion posi-tive staining with lysozyme and a1AT in combina-tion with other diagnostic criteria, can be helpful inthe diagnosis of fibrous histiocytomas. Alpha-i-antichymotrypsin, however, would appear to be anunreliable marker in these tumours.The salivary gland adenomas of predominantly

spindled cell pattern, attributed to the myoepithelialcomponent,22 are the tumours for which fibrous his-tiocytomas are most likely to be mistaken.48 Epithel-ial structures may be scanty and unless multiple sec-tions are taken, may be entirely missed. Four spin-dled cell variants of mixed salivary tumour studiedfor histiocytic markers were found to be negative forlysozyme and a,AT in contrast to the fibrous his-tiocytomas. Therefore in unusual locations, such asthe salivary glands, these markers can be particu-larly useful in differential diagnosis.Neurilemmoma, neurofibroma and leiomyoma

are rare salivary gland tumours which might bear asuperficial resemblance to a benign fibrous his-tiocytoma whilst various sarcomas, including rhab-domyosarcoma and fibrosarcoma, have to be distin-guished from malignant fibrous histiocytoma. Elec-tron microscopy has a valuable role to play in theprecise diagnosis of these spindled cell neoplasms.

References

' Thackray AC, Sobin LH. Histological typing of salivary glandtumours. Geneva: World Health Organisation, 1972;7:25.

2 Sternberger LA, Hardy PH, Cuculus JJ, Meyer HG. The unlabel-led antibody enzyme method of immunohistochemistry. Prep-aration and properties of the soluble antigen-antibody com-plex (horseradish peroxidase anti-horseradish peroxidase) andits use in identification of spirochetes. J Histochem Cytochem1970;18:315-33.

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3 O'Brien JE, Stout AP. Malignant fibrous xanthoma. Cancer1964;17: 1445-55.

4 Junaid TA, Ani AN, Ejeckam GC. Dermatofibrosarcoma pro-truberans in the parotid gland - a case report. Br J Oral Surg1975;12:298-301.

Blitzer A, Lawson W, Biller HF. Malignant fibrous histiocytomaof the head and neck. Laryngoscope 1977;87:1479-99.

6 Nilsen R, Lind 0. Benign fibrous xanthoma of the parotid gland:a case report. Br J Oral Surg 1978-79;16:111-4.

7 Shapshay SM, Wingert RH, Davis JS. Fibrous histiocytoma ofthe parotid gland. Laryngoscope 1979;89:1808-12.

Fayemi AO, Ali M. Fibrous histiocytoma of the parotid gland.Mt Sinai J Med (NY) 1980;47:290-2.

Weiss SW, Enzinger FM. Malignant fibrous histiocytoma. Ananalysis of 200 cases. Cancer 1978;41:2250-66.

'° Hoffbrand AV, Lewis SM. Postgraduate haematology. 2nd ed.London: William Heineman Medical Books Ltd, 1981:484.

" Ozello L, Stout AP, Murray MR. Cultural characteristics ofmalignant histiocytomas and fibrous xanthomas. Cancer1963;16:331-44.

12 Jacob F. Cells and tissues in culture: methods, biology andphysiology. London and New York: Academic Press,1965;2:78.

3 Alguacil-Garcia A, Unni KK, Goellner JR. Malignant fibroushistiocytoma. An ultrastructural study of six cases. Am J ClinPathol 1978;69:121-9.

4 Yumoto T, Morimoto K. Experimental approach to fibrous his-tiocytoma. Acta Pathol Jpn 1980;30:767-78.

5 Fu YS, Gabbiani G, Kaye GI, Lattes R. Malignant soft tissuetumours of probable histiocytic origin (malignant fibrous his-tiocytomas): general considerations and electron microscopicand tissue culture studies. Cancer 1975;35:176-98.

16 Taxy JB, Battifora H. Malignant fibrous histiocytoma. An elec-tron microscopic study. Cancer 1977;40:254-67.

"1 Harris M. The ultrastructure of benign and malignant fibroushistiocytomas. Histopathology 1980;4:29-44.

Im Churg AG, Kahn LB. Myofibroblasts and related cells in malig-nant fibrous and fibrohistiocytic tumours. Hum Pathol1977;8:205-18.

'9 Mason DY, Taylor CR. The distribution of muramidase(lysozyme) in human tissues. J Clin Pathol 1975;28: 124-32.

20 Meister P, Konrad EA, Nathrath W, Eder M. Malignant fibroushistiocytoma: histological patterns and cell types. Pathol ResPract 1980;168:193-212.

21 Isaacson P, Jones DB, Millward-Sadler GH, Judd MA, Payne S.Alpha-i -antitrypsin in human macrophages. J Clin Pathol1981;34:982-90.

22 Merino MJ, Li Volsi VA. Pleomorphic adenomas of the parotidgland resembling mesenchymal tumours. Oral Surg1977;44:405-1 0.

Requests for reprints to: Professor H Fox, Department ofPathology, University of Manchester, Stopford Building,Oxford Road, Manchester M13 9PT, England.

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Malignant fibrous of salivary glands - From BMJ and ACP · malignant fibrous histiocytoma arising in salivary glands are presented andthe features ofseven previouslyreportedcasesare