Desmoplastic variant of ameloblastoma in Chinese patients

Desmoplastic variant of ameloblastoma in Chinese patients

- Desmoplastic variant of ameloblastoma in Chinese patients K. Y. Lam, A. C. L. Chan, F?C. Wu, K. Y. Chau, H. Tideman, W. Wei Departments of Patholog...

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Desmoplastic variant of ameloblastoma in Chinese patients K. Y. Lam, A. C. L. Chan, F?C. Wu, K. Y. Chau, H. Tideman, W. Wei Departments of Pathology and Surgery, Queen Mary Hospital, Hongkong: Department of Oral and Maxillofacial Surgery, Prince Philip Dental Hospital, Hong Kong SUMMARY. Desmoplastic ameloblastoma is a rare tumour, and we know of only 43 previously reported cases. We report seven Chinese patients (five men and two women) with the desmoplastic variant of ameloblastoma, which makes up 9% of all ameloblastomas diagnosed during the years 1981-1995. The age ranged from 18 to 68 years (mean 43). Five of the tumours were in the maxilla and two were in the mandible. Five of them were situated anteriorly, the remaining two cases involving both anterior and posterior maxilla. The features of the 42 cases previously reported were reviewed and were comparkd with those in the present study. Our results differ in that we found a male predominance, wider age range and more tumours in the maxilla. Histologically, this variant of ameloblastoma is characterized by abundant collagenous stroma. Because the epithelial clusters may show prominent squamous metaplasia or may be compressed into thin strands in most areas, the appearance may mimic a squamous odontogenic tumour or odontogenic fibroma. The behaviour of this variant of ameloblastoma is likely to be the same as that of the classic ameloblastoma.

INTRODUCTION

RESULTS

Ameloblastoma is a relatively rare benign tumour of the jaws which is locally invasive.’ Different pathological patterns have been described and these include follicular, plexiform, unicystic, acanthomatous, granular cell and basal ce11.2Apart from the unicystic type (which has a lower recurrence rate),3 there are no significant differences in behaviour among the other histological types. In 1984, Eversole et a1.4 first reported three cases of ameloblastoma with pronounced desmoplastic stroma and subsequent case reports and series supported the identification of this sub-group.5m14 In the present study we have aimed to identify the occurrence and characteristic of this subtype of ameloblastoma in our local Chinese population, and compared the findings with those of previous reports.

There were 81 Chinese patients with ameloblastoma. Of these, seven (including two previously reported elsewhere)14 of the desmoplastic variant were identified, accounting for 9% of all ameloblastomas diagnosed in our department (Table 1). The patients presented with painless swelling of the face or alveolus. In case 1, the history should be treated with reserve because it is unlikely that the tumour remained so small (2 cm) after 20 years. Radiologically, cases 1 to 5 had areas of radiolucency with a ‘soap-bubble’ appearance (Fig. 1). Radiolucent lesions with some abnormal trabecula patterns were noted in cases 6 and 7 (Fig. 2). Grossly, all the tumours originated in the bone and had breached the cortical plates. They ranged from 1.8 cm to 6 cm in maximum dimension (mean: 3.9) and were firm in consistency. The cut surfaces were solid and homogeneously whitish (Fig. I), but a few small cystic areas were identified focally in two cases (cases 1 & 3). The cysts were up to 0.5 cm in diameter in case 3. Histologically, all the tumours were unencapsulated and had breached the cortical plates. Ameloblastic epithelium was embedded within abundant collagenous fibrous stroma in all cases. In some areas, the epithelium was compressed into narrow strands (Fig. 3). A peripheral palisading layer of columnar cells with cytoplasmic vacuolation, hyperchromatic nuclei and reverse polarization characteristic of ameloblastoma was present in only some of the epithelial clusters. In all cases, the centre of the epithelial clusters was composed of regular oval or spindle cells with focal squamous metaplasia. Some showed

PATIENTS AND METHODS The files from the Department of Pathology of the University of Hong Kong were reviewed to find out the incidence of ameloblastoma during the 15-year period from January 1981 to December 1995. Only tumours from Chinese patients were chosen for further analysis. The histological sections were then reviewed to find out the incidence of desmoplastic ameloblastoma in our local population. The basic diagnostic criteria of this variant were those defined by Eversole et al.4 In addition, the clinical records of the patients were retrieved and the clinicopathological characteristics, including the follow-up data were analysed. 129

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Table 1 - Clinical details of seven cases of desmoplastic variant of ameloblastoma. Case No.

Sex/age (years)

1

F/68

2

Site

Size (cm)

Main complaint

Operation

Remarks

Right maxilla/anterior

2.0

Maxillary swelling for 20 years

Enucleation

F/31

Bilateral mandible/anterior

2.5

Gum swelling for 4 months

Segmental mandibulectomy

3*

M/2 1

Right maxilla/anterior

4.0

Cheek swelling for 2 weeks

Right maxillectomy

4*

Ml53

Left maxilla/extensive

5.0

Facial swelling for 1.5 years

Left maxillectomy

5

M/18

Left maxilla/anterior

6.0

Maxillary swelling for 9 months

Left maxillectomy

6

Ml37

Bilateral maxilla/anterior

1.8

Gum swelling for 2 weeks

Marginal mandibulectomy

I

Ml64

Left maxilla/extensive

6.0

Gum swelling for a few months

Left maxillectomy

Recurrence 74 months after enucleation; limited resection of alveolar process of maxilla; no residual disease 5 years 10 months after second operation No residual disease 6 years and 5 months after operation No residual disease 4 years and 6 months after operation No residual disease 5 years and 1 month after operation No residual disease 4 years and 5 months after operation No residual disease 2 years and 8 months after operation Case being treated by a private doctor before admission and had two recurrences within two years. No residual disease 1 year and 7 months after maxillectomy

*Reported in a previous study.13

microcytic changes. There was also a thin rim of loose myxoid stroma around at least some epithelial nests in all cases. In five cases, this was focal periepithelial induction (deposition of a thin layer of acellular eosinophilic matrix). Elastin van Giesen stain failed to show any elastic fibre within the desmoplastic stroma. Only two tumours (in cases 1 and 7) recurred. Case 1 recurred 6.2 years after enucleation. Case 7 was treated by limited local excision. The patient had two recurrences within 2 years of presentation, The recurrent lesion in case 1 was treated by partial maxillectomy while case 7 was treated by maxillectomy. No recurrences were detected in any cases (including cases 1 and 7) after curative resection (median follow-up 4.5 years, range 1.6-6.4).

DISCUSSION

The desmoplastic variant of ameloblastoma was first described by Eversole et a1.4in 1984 and since then we have found reports of 43 cases (Table 2).&13 The incidence of this variant of ameloblastoma in four previous series was 0.9% 4%, 5.2% and 12.1% of all ameloblastomas.s~8~11~12 In the present study, the incidence was 9% (7/81), so the incidence in Hong Kong Chinese is second only to that reported by Waldron et al5 However, the high incidence in the report by Waldron et al. 5 might be influenced by the addition of cases from the personal collection of one of the authors.

Despite the unknown racial origin of 11 of the cases reported by Waldron et a1.,5 desmoplastic ameloblastoma has been detected mainly in Chinese (n = 13; 6 Malaysian Chinese and 7 Hong Kong Chinese), Malaysians (n = 7), Afro-Caribbean (n = 7) and Japanese (n = 5) (Table 3).h13 On the whole, desmoplastic ameloblastoma is slightly more common among women (16 men, 26 women, 1 sex not mentioned; M:F ratio 1:1.6). The female predominance was seen in all ethnic groups, particularly the Malaysian Chinese.” Our series (composed entirely of Hong Kong Chinese patients), however, differs by showing a male predominance (2.5: 1). Interestingly, many authors have reported an even distribution between the sexes or a male preponderance in classic ameloblastoma.15 Classic ameloblastoma in adults presents predominantly in the third to fifth decades.*,15 The ages of patients with desmoplastic ameloblastomas were similar, ranging from 21 to 68 years (mean 41), with 88% of the patients in the third to fifth decades. The present series in that there is a wider age range (18-68, mean 43); case 5 is the youngest reported patient that we had and case 1 is the eldest. Among the sites of the 43 previously reported cases, there was a slight predominance of the mandible (mandible vs. maxilla, 56% and 44%). This is in contrast to ameloblastoma in general in which a much higher percentage (85-95%) of cases develop in the mandible.15-l7 Our results in Chinese patients are similar to those in Malaysian series,” and show a

Desmoplastic

ameloblastoma

Fig. 2 - Radiograph showing a mixed radiolucent lesion with ill-defined borders (arrows).

Fig. 1 ~ Radiograph appearance.

showing

a lesion

with

‘soap

13 1

and radiopaque

bubble’

predominance of the maxilla (2.5:l). Like previous authors,4JJJ0J’ we also found a high incidence in the anterior part of the jaws with involvement of the alveolar bone in every case. The reason for the high percentage of tumours with maxillary involvement and invasion of the anterior part of the tooth-bearing jaws is unknown. The local environment may allow the tumour islands to elicit a particular desmoplastic response within the stroma. Nevertheless, other as yet unknown factors are likely to be involved because other variants of ameloblastoma also occur at these sites. The radiological features of the desmoplastic variant have been reviewed by Kaffe et a1.9 Radiologically, many cases (including cases 6 and 7 in the present study) had a mixed radiolucent-radiopaque appearance and showed poorly-defined or diffuse borders that suggested libro-osseous lesions. In our series, five cases were radiolucent with a ‘soap-bubble’ appearance, similar to classic cases of ameloblastoma. In case 6, there was no radiological evidence of bony involvement but the gross specimen showed that the origin was definitely the tooth-bearing bone of the mandible. In this series we have included only those cases in which the predominant histological pattern of the

Fig. 3 ~ The tumour has abundant collagenous stroma and the epithelial nests are compressed into thin strands. The central cluster shows a peripheral palisading layer of columnar cells that is characteristic of ameloblastoma together with squamous metaplasia. A thin rim of myxomatous stroma is present around the epithelial nests. (Haematoxylin and eosin; original magnification x 165.)

tumour shows a desmoplastic reaction. Apart from this, focal areas similar to the desmoplastic variant may occur in otherwise typical plexiform, follicular, acanthomatous, or any other types of ameloblastoma. Such tumours can be classified as the hybrid tumours as reported by Waldron et al. 5 and Higuchi et al. *

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Table 2 - Previously reported cases of desmoplastic ameloblastoma Author\year\ethnic

group

Eversole\l984\White Eversole\l984\ Afro-Caribbean Eversole\l984\Malaysian Wadron\1987\ 3 Afro-Carribbean (other not known)

Sex/age

Site

F/50 F/41 F/48 7M, 7Fl (F/21, 32, 35, other not known) 45.5 (21-68)

Treatment

Follow-up

Mandible/anterior Mandible/anterior

Not known En bloc excision

Not known Not known

Maxilla/extensive

Maxillectomy

7 Maxilla (6 anterior/l posterior), 7 Mandible (2 anterior/ 5 posterior)

Not known

2 years no evidence of disease of disease 1 recurrence 2 years after curettage; 1 recurrence (details not known); 1: 1 year with no evidence of disease 11 not known 9 years with no evidence of disease 1 year with no evidence of disease Not known

Yoshimura\l990Vapanese

F/36

Maxilla/extensive

Maxillectomy

Tanimoto\l991Dapanese

F124

Mandible/extensive

Marginal resection

Higuchi\l991Uapanese

Ml46 F/38 M/53 Ml41

Maxilla/anterior Mandible/anterior Mandible/anterior Maxilla/extensive

Enucleation Enucleation Enucleation Maxillectomy

Ashman\1993\ Afro-Caribbean Ng\l993\Chinese Ng\l993\Chinese Ng\l993\Malaysian Ng\l993\Chinese Ng\l993\Kadazan Ng\l993\Indian Ng\l993\Malaysian Ng\l993\Malaysian

M/53

Mandible/anterior

Marginal resection

F/21 Ml25 M/25 F/21 F/29 F/32 Ml33 F/33

Mandible/anterior Maxilla/ ~ Mandible/anterior Mandible/anterior Mandible/extensive Maxilla/anterior Maxilla/anterior Maxilla/extensive

Marginal resection Maxillectomy Excision Not known Resection Not known Not known Maxillectomy

Ng\l993\Malaysian Ng\l993\Chinese Ng\l993\Malaysian Ng\l993\Chinese Ng\l993\Malaysian Ng\l993\Chinese Ng\l993\Indian Ng\1993\Sikh

M/38 F/40 F/41 F/42 F/43 F/43 F/44 F/46

Maxilla/anterior Mandible/anterior Maxilla/anterior Mandible/posterior Mandible/anterior Mandible/anterior Mandible/anterior Maxilla/ ~

Excision Not known Excision Not known Not known Not known Segmental resection Maxillectomy

Ng\l993\Chinese Raubenheimer\l995\ Afro-Caribbean Thompson\l996\ Afro-Caribbean

M/60

Mandible/anterior

Not known

3 years with no evidence of disease 9 months with no evidence of disease Not known Not known Not known Not known Not known Not known Not known 1 year with no evidence of disease Not known Not known Not known Not known Not known Not known Recurrence after 4 years 1 year with no evidence of disease Not known

-IF131

Mandible/Maxilla/anterior

Not known Maxillectomy

Not known Not known

Kaffe\l993\Israeli

Table

3 - Characteristics of desmoplastic ameloblastoma in different ethnic group

Ethnic group Malaysian Chinese (n = 7) Malaysian (n = 7) Japanese (n = 5) Black (n = 6) Hong Kong Chinese (n = 7)

Sex ratio (M:F)

Mean age (years) (range)

215 3:4 213 1:5 512

37 (21-60) 37 (2548) 39 (24-53) 33 (2147) 43 (18-68)

Histologically, the tumour might be misdiagnosed as another odontogenic tumour, as the characteristic palisading layer of ameloblastoma may not be present in all the epithelial clusters, particularly if the biopsy specimen is small. Areas with only narrow strands of epithelial cells within desmoplastic stroma may simulate odontogenic fibroma, a tumour composed of inactive odontogenic epithelium embedded within the fibrous tissue.18J9 The importance lies in the differences in the clinical behaviour and management of these two tumours. Ameloblastoma is a potentially

Site 1 maxilla/6 5 maxilla/2 2 maxilla/3 4 maxilla/2 5 maxilla/2

mandible mandible mandible mandible mandible

aggressive tumour that requires en bloc resection (which may mean maxillectomy or mandibulectomy). Odontogenic fibroma is much less aggressive and enucleation is probably curative. Accurate diagnosis of the desmoplastic variant of ameloblastoma depends on the identification of the typical ameloblastic areas, and this may require examination of more tissue or a repeated biopsy. Another differential diagnosis is squamous odontogenie tumour.2S22 As this may have a fibrotic stroma, the squamous metaplasia observed in some areas of

Desmoplastic

the desmoplastic variant of ameloblastoma may mimic it if the palisading layer of the tall columnar cells is not identified. Goldblatt et ~1.~’ reported no myxomatous change or other inductive effects in the connective tissue surrounding the epithelial clusters in squamous odontogenic tumour, and this feature may be useful in doubtful cases. All our cases of the desmoplastic variant of ameloblastoma showed peripheral palisading layer of columnar cells and thin rim of periepithelial myxoid stroma at least focally. Five of the seven cases showed inductive effects with deposition of an acellular eosinophilic matrix around the epithelial islands. Like odontogenic fibroma, an accurate diagnosis is important not only for academic interest, but also because the management is different. Although some cases of squamous odontogenic tumour may have an aggressive clinical course, the currently preferred treatment is curettage, which is followed by few recurrences. Other differential diagnoses include squamous cell carcinoma and ameloblastic tibroma. The former has prominent cytological atypia while the latter has a cellular stroma. Classic ameloblastoma, as reported by Muller and Slootwegz3 usually recurs within 5 years of the initial treatment. In previously reported cases of desmoplastic ameloblastoma, the follow-up period was usually short (9 months to 4 years) or there were no follow-up data at a11.4m1jThe only exception was the case reported by Yoshimura and Setoh in which there was no evidence of recurrence 9 years after operation. Unlike the previous studies, follow-up information was available for all of our cases and the median follow-up period after the definitive operation was more than 4 years (54 months). The clinical behaviour of a desmoplastic ameloblastoma is similar to the usual ameloblastoma. Limited local treatment is not adequate, and may be followed by recurrence (as illustrated by cases 1 and 7). En bloc resection is the treatment of choice. The effectiveness of treatment could be reflected by the lack of recurrence in all the cases with en bloc excision although a longer follow-up period may be necessary in the two recent cases (cases 6 and 7, whose disease-free periods were 32 and 19 months after the operation) before we can comment more definitely. In summary, as well as the histological characteristics, desmoplastic variant of ameloblastoma differs clinically from the usual ameloblastoma by more commonly developing in the anterior part of the jaws. There is also a male preponderance in our series, a wide age range, and more tumours in the maxilla. The clinical behaviour was similar to that of the usual ameloblastoma with recurrence occurring after local enucleation but not after en bloc resection. Histologically, the tumour may be mimicked by the less aggressive odontogenic fibroma or squamous odontogenic tumour. References 1. Kramer IRH, Pindborg JJ, Shear M. Histological typing of odontogenic turnouts. 2nd ed. Berlin: Springer-Verlag, 1992: 1 l-14.

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2. Williams TP. Management of ameloblastoma: a changing perspective. J Oral Maxillofac Surg 1993; 51: 1064-1070. 3. Ackermann GL, Altini M, Shear M. The unicystic ameioblastoma: a clinicopathological study of 57 cases. J Oral Pathol 1988; 17: 541-546. 4. Eversole LR, Leider AS, Hansen LS. Ameloblastomas with pronounced desmoplasia. J Oral Maxillofac Surg 1984; 42: 7355740. 5. Waldron CA, El-Mofty SK. A histopathological study of 116 ameloblastomas with special reference to the desmoplastic variant, Oral Surg Oral Med Oral Pathol 1987; 63: 441-451. 6. Yoshimura Y, Saito H. Desmoplastic variant of ameloblastoma: report of a case and review of the literature. J Oral Maxillofac Surg 1990; 48: 1231-1235. I. Tanimoto K, Takata T, Suei Y, Wdda T. A case of desmoplastic variant of a mandibular ameloblastoma. J Oral Maxillofac Surg 1991; 49: 9497. 8. Higuchi Y, Nakamura N, Ohishi M, Tashiro H. Unusual ameloblastoma with extensive stromal desmoplasia. J Craniomaxillofac Sum 1991: 19: 323-327. 9. Kaffe 1, Buchner A, TaGher S: Radiological features of desmoplastic variant of ameloblastoma. Oral Surg Oral Med Oral Pathol 1993; 76: 5255529. 10. Ashman SC, Corio RL, Eisele DW, Murphy MT. Desmoplastic ameloblastoma: a case report and literature review. Oral Surg Oral Med Oral Pathol 1993; 75: 479482. Il. Ng KH, Siar CH. Desmoplastic variant of ameloblastoma in Malaysians. Br J Oral Maxillofac Surg 1993; 3 1: 2999303. 12. Raubenheimer EJ, van Heerden WFP Noble CEE. Infrequent chnicopathological findings in 108 ameloblastomas. J Oral Pathol Med 1995; 24: 2277232. 13. Thomoson IOC. van Rensburg LJ. Phillios VMJ. Desmoolastic ameloblastoma: correlative histopathology, radiology and CT-MR imaging. J Oral Patho1 Med 1996; 25: 405410. 14. Philipsen HP, Ormiston IW, Reichart PA. The desmo- and osteoplastic ameloblastoma. Histological variant or clinicopathological entity? Case reports. Int J Oral Maxillofac Surg 1992: 21: 352-357. 15. Olaitan AA. Adeola DS, Adekeye EO. Ameloblastoma: clinical features and management of 315 cases from Kaduna, Nigeria. J Craniomaxillofac Surg 1993; 21: 351-355. 16 Ueno S, Nakamura S, Mushimoto K, Shirasu R. A clinicopathological study of ameloblastoma. J Oral Maxillofac Surg 1986; 44: 361-365. 17. Regezi JA, Sciubba JJ. Oral pathology, clinical-pathologic correlations. Philadelphia: WB Saunders, 1993: 3622367. 18 Kramer IRH, Pindborg JJ. Shear M. Histological typing of odontogenic tumours. 2nd ed. Berlin: Springer-Verlag, 1992: 22. 19 Sciubba JJ. Central odontogenic tibroma of the WHO type. Oral Surg Oral Med Oral Path01 1984; 57: 390-394. 20. Kramer IRH, Pindborg JJ, Shear M. Histological typing of odontogenic tumours. 2nd ed. Berlin: Springer-Verlag. 1992: 14. 21 Goldblatt LI, Brannon RB, Ellis GL. Squamous odontogenic tumour, report of five cases and review of the literature. Oral Surg Oral Med Oral Path01 1982; 54: 187.-196. 22 Leventon GS, Happonen R-P, Newland JR. Squamous odontogenic tumour, report of two cases and review of the literature. Am J Surg Path01 1981; 5: 671-677. 23. Muller H, Slootweg PJ. The growth characteristic of multilocular ameloblastomas. J Maxillofac Surg 1985; 13: 224-230.

The Authors K. Y. Lam FRCPA Honorary Lecturer Alexander C. L. Chan FRCPA Senior Medical Officer P.C.WuMD Professor K. Y. Chau MRCPath Senior Medical Officer Department of Pathology

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Correspondence and requests for offprints to Dr K.Y. Lam, Department of Pathology, Queen Mary Hospital, Pokfulam Road, Hong Kong

(Professor)

Department of Surgery Queen Mary Hospital Hong Kong He&

Tide&an

MD,

PhD

Professor Department of Oral and Maxillofacial Prince Philip Dental Hospital Hong Kong

Surgery

Surgery

Paper received 8 July 1996 Accepted 8 March 1997