fine-needle aspiration cytology of adenoid cystic carcinoma of the breast

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Fine-Needle Aspiration Cytology of Adenoid Cystic Carcinoma of the Breast Raj K. Gupta, M.D., F.I.A.C., 1 * Carol Green, C. (F.I.A.C.), 2 Sarla Naran, B.Sc., C.M.I.A.C., 1 Sharda Lallu, B.Sc., C.M.I.A.C., 1 Robert Fauck, C.T. (I.A.C.), 1 Carl Dowle, M.B., Ch.B., F.R.A.C.S., 3 and John Simpson, M.B., Ch.B., F.R.A.C.S., F.R.C.S. 3 Adenoid cystic carcinoma (ACC) of the breast is a rare variant of breast malignancy and has a better prognosis than its counterpart in the salivary glands. In this communication, our experience with seven cases of ACC of the breast is presented in which the diagnosis was established on fine-needle aspiration cytology (FNAC). The cytologic samples in all cases were cellular and featured three-dimensional clusters of uniform ductal epithelial cells with cystic spaces, bland nuclei, fine chromatin, and scanty cytoplasm arranged around spheres or cores of homogenous material. The cytodiagnosis of ACC in all cases correlated with subsequent examination of cell blocks of the aspirate and tissue. The cytodiagnostic criteria for ACC of the breast which are useful in a correct FNAC diagnosis are discussed. Diagn. Cytopathol. 1999;20:82–84. r 1999 Wiley-Liss, Inc. Key Words: breast; fine-needle aspiration cytology; adenoid cystic carcinoma Adenoid cystic carcinoma (ACC) of the breast is a rare variant of breast malignancy with a good prognosis and its incidence is less than 1% of all breast carcinomas. Its morphological features are identical to similar malignancies which rarely occur in salivary and lacrimal glands, nasal cavity, lung, trachea, cervix, and Bartholin’s gland. Al- though the histologic features of ACC have been well known, its features in cytologic material have only been reported in a few case studies. 1–15 In this communication, we present our total experience with seven cases of ACC of the breast which were seen over a period of 15 yr and in which the distinctive appearance of the tumor cells in fine-needle aspiration cytologic (FNAC) samples enabled the cytodiagnosis to be made without any difficulty. The FNAC findings in all cases were further correlated with the histologic architecture of ACC, which was seen on subsequent examination of cell block from the aspirate and breast tissue. As far as we are aware, a large study of FNAC diagnosis of ACC of the breast has not been reported to date in the English literature. The cases were also seen in conjunction with Dr. Tilde S. Kline of Philadelphia, PA, during her recent visit to our laboratories in Wellington and Lower Hutt, New Zealand. Materials and Methods From January 1983 to February 1998, 20,487 fine-needle aspirates of the breast from patients between 15 and 96 yr of age were examined cytologically; from these, seven were from women in which an FNAC diagnosis of ACC was made. The pertinent information in all seven cases was obtained from the clinician and by further review of the charts for details of clinical, surgical, and other information, which are summarized in Table I. All needle aspirates were obtained using a disposable 10 ml syringe and 22 gauge needle. Aspirations were performed using multiple passes in the breast mass, maintaining negative pressure. For cytologic study, washings were prepared from aspirated sample by immediately washing the syringe and needle contents in a cytology container in which 30% ethyl alcohol in physiologic saline was present. This was accomplished by withdrawing the 30% ethyl alcohol in the syringe barrel, and with the needle attached, flushing the contents back into the cytology container and repeating this procedure three times for maximum recovery of the mate- rial. From these washings, cytologic preparations were made on membrane filters (size 22 mm; pore size 3 μm). The staining was done by Papanicolaou method. For histologic study, cell blocks from the aspirate and the excised breast tissue were first fixed in 10% neutral buffered formalin for 72 hr, and following gross examination of the tissue, representative samples from the mass and surround- 1 Cytology Unit, Wellington Hospital, Wellington, New Zealand 2 Cytology Unit, Valley Diagnostic Laboratory Ltd., Lower Hutt, New Zealand 3 Department of Surgery, Bowen and Hutt Hospitals, Wellington and Lower Hutt, New Zealand *Correspondence to: Raj K. Gupta, M.D., F.I.A.C., Cytology Unit, Wellington Hospital, Wellington, New Zealand. Received 1 April 1998; Accepted 21 July 1998 82 Diagnostic Cytopathology, Vol 20, No 2 r 1999 WILEY-LISS, INC.

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Page 1: Fine-needle aspiration cytology of adenoid cystic carcinoma of the breast

Fine-Needle Aspiration Cytologyof Adenoid Cystic Carcinoma ofthe BreastRaj K. Gupta, M.D., F.I.A.C.,1* Carol Green, C. (F.I.A.C.),2 Sarla Naran, B.Sc.,C.M.I.A.C.,1 Sharda Lallu, B.Sc., C.M.I.A.C.,1 Robert Fauck, C.T. (I.A.C.),1 CarlDowle, M.B., Ch.B., F.R.A.C.S.,3 and John Simpson, M.B., Ch.B., F.R.A.C.S., F.R.C.S.3

Adenoid cystic carcinoma (ACC) of the breast is a rare variant ofbreast malignancy and has a better prognosis than its counterpartin the salivary glands. In this communication, our experience withseven cases of ACC of the breast is presented in which thediagnosis was established on fine-needle aspiration cytology(FNAC). The cytologic samples in all cases were cellular andfeatured three-dimensional clusters of uniform ductal epithelialcells with cystic spaces, bland nuclei, fine chromatin, and scantycytoplasm arranged around spheres or cores of homogenousmaterial. The cytodiagnosis of ACC in all cases correlated withsubsequent examination of cell blocks of the aspirate and tissue.The cytodiagnostic criteria for ACC of the breast which are usefulin a correct FNAC diagnosis are discussed.Diagn. Cytopathol.1999;20:82–84. r 1999 Wiley-Liss, Inc.

Key Words:breast; fine-needle aspiration cytology; adenoid cysticcarcinoma

Adenoid cystic carcinoma (ACC) of the breast is a rarevariant of breast malignancy with a good prognosis and itsincidence is less than 1% of all breast carcinomas. Itsmorphological features are identical to similar malignancieswhich rarely occur in salivary and lacrimal glands, nasalcavity, lung, trachea, cervix, and Bartholin’s gland. Al-though the histologic features of ACC have been wellknown, its features in cytologic material have only beenreported in a few case studies.1–15

In this communication, we present our total experiencewith seven cases of ACC of the breast which were seen overa period of 15 yr and in which the distinctive appearance ofthe tumor cells in fine-needle aspiration cytologic (FNAC)samples enabled the cytodiagnosis to be made without any

difficulty. The FNAC findings in all cases were furthercorrelated with the histologic architecture of ACC, whichwas seen on subsequent examination of cell block from theaspirate and breast tissue. As far as we are aware, a largestudy of FNAC diagnosis of ACC of the breast has not beenreported to date in the English literature. The cases were alsoseen in conjunction with Dr. Tilde S. Kline of Philadelphia,PA, during her recent visit to our laboratories in Wellingtonand Lower Hutt, New Zealand.

Materials and MethodsFrom January 1983 to February 1998, 20,487 fine-needleaspirates of the breast from patients between 15 and 96 yr ofage were examined cytologically; from these, seven werefrom women in which an FNAC diagnosis of ACC wasmade. The pertinent information in all seven cases wasobtained from the clinician and by further review of thecharts for details of clinical, surgical, and other information,which are summarized in Table I.

All needle aspirates were obtained using a disposable 10ml syringe and 22 gauge needle. Aspirations were performedusing multiple passes in the breast mass, maintainingnegative pressure. For cytologic study, washings wereprepared from aspirated sample by immediately washing thesyringe and needle contents in a cytology container in which30% ethyl alcohol in physiologic saline was present. Thiswas accomplished by withdrawing the 30% ethyl alcohol inthe syringe barrel, and with the needle attached, flushing thecontents back into the cytology container and repeating thisprocedure three times for maximum recovery of the mate-rial. From these washings, cytologic preparations were madeon membrane filters (size 22 mm; pore size 3 µm). Thestaining was done by Papanicolaou method.

For histologic study, cell blocks from the aspirate and theexcised breast tissue were first fixed in 10% neutral bufferedformalin for 72 hr, and following gross examination of thetissue, representative samples from the mass and surround-

1Cytology Unit, Wellington Hospital, Wellington, New Zealand2Cytology Unit, Valley Diagnostic Laboratory Ltd., Lower Hutt, New

Zealand3Department of Surgery, Bowen and Hutt Hospitals, Wellington and

Lower Hutt, New Zealand*Correspondence to: Raj K. Gupta, M.D., F.I.A.C., Cytology Unit,

Wellington Hospital, Wellington, New Zealand.Received 1 April 1998; Accepted 21 July 1998

82 Diagnostic Cytopathology, Vol 20, No 2 r 1999 WILEY-LISS, INC.

Page 2: Fine-needle aspiration cytology of adenoid cystic carcinoma of the breast

ing breast tissue were taken and processed, embedded, cut at5 µm, and stained with hematoxylin-eosin (H&E). Inaddition, sections of cell block and tumor tissue were alsostained with mucicarmine and Alcian blue (pH 2.5).

ResultsPapanicolaou-stained filter preparation and H&E-stainedsections of cell block preparations from aspirate and excisedbreast tissue with the tumor showed three-dimensionalclusters of uniform ductal cells with cystic spaces. Thenuclei were bland and uniform, small and ovoid, with finechromatin and scanty cytoplasm (Figs. 1A,B, 2) arrangedaround cores or spheres of homogenous acellular or metachro-matic material. The cystic spaces contained cyanophilicamorphous material that stained positive for mucin onmucicarmine and Alcian blue stains. Pertinent details ofclinical and other information on the seven cases is sum-marised in Table I.

DiscussionACC is known to occur in salivary glands, breast, lung, nasalcavity, skin, trachea, cervix, and lacrimal gland. The behav-ior of ACC of salivary gland is more aggresive. Thediagnosis of ACC in needle aspirate from the breast isimportant to enable timely management since the prognosisof ACC in the breast is generally better than its counterpartin other sites like the salivary gland and in comparison toother breast carcinomas.16,17 Also, its recognition is very

desirable from FNAC samples, which are becoming morecommon as a first line of investigation for diagnosis of alltypes of breast abnormalities. Therefore, it is of paramountimportance that the cytopathologist keep the features of thisrare breast tumor in mind, especially if the FNAC sample ishighly cellular with abundant clusters of small cells withround, monotonous, hyperchromatic nuclei and scanty cyto-plasm arranged around cores of acellular homogenousmaterial. In differential diagnosis, an exclusion of other

Table I. Summary of Findings in Seven Cases of ACCa

Caseno.

Age(yr)

Pertinent clinicalfindings Cytology Management Histology

1 52 3.53 2 cm partly cystic firmmass in right upper outerquadrant of breast

ACC WLE ACC (C, T)

2 38 2.53 2.5 cm firm mass inright lower outer quadrantof breast

ACC WLE ACC (C, T)

3 69 1.83 1.5 cm rubbery massin left upper outer quad-rant of breast

ACC WLE ACC (C, T)

4 42 1.53 1 cm discrete firmmass in right upper outerquadrant of breastdetected on mammog-raphy

ACC WLE ACC (C, T)

5 49 1.23 1 cm discrete mass inleft lower outer quadrantof breast detected onmammogram

ACC WLE ACC (C, T)

6 53 9.53 8.5 cm partly cysticfirm mass occupyingabout half of left breast

ACC Mastectomy ACC (C, T)

7 45 4.53 2.5 cm firm mass inright upper inner quadrantof breast

ACC WLE ACC (C, T)

aWLE, wide local excision; C, cell block; T, tissue.

Fig. 1. A: Low-power view of Papanicolaou-stained filter preparationshowing a tissue fragment in cellular aspirate of ACC with clusters ofuniform ductal cells with cystic spaces (Papanicolaou,3350). B: High-power view of A in another field in the aspirate sample with clusters ofuniform ductal cells with cystic spaces (Papanicolaou,3750).

Fig. 2. Cell block of aspirate showing histologic features of ACC withcystic spaces containing mucus (H&E,3350).

ADENOID CYSTIC CARCINOMA OF THE BREAST

Diagnostic Cytopathology, Vol 20, No 2 83

Page 3: Fine-needle aspiration cytology of adenoid cystic carcinoma of the breast

common breast carcinomas—carcinoid, lymphoma, collag-enous spherulosis, myospherulosis, and cribiform intra-ductal or pseudoadenoid cystic carcinoma—may be neces-sary. As these conditions have been adequately discussed indetail and emphasized in recent studies12,13,18,19to which weagree, these are not discussed in this presentation.

In summarizing, it is felt that the diagnosis of ACC inFNAC samples, despite its rarity, should not be difficult,especially if some of its recently described criteria13 such asclinical mass, cellular smears comprising small, uniformmonotonous cells with scanty cytoplasm, and fine chromatinare present. In addition, the arrangement of tumor cellsaround cores or spheres of homogenous acellular materialand the presence of cystic spaces with cyanophilic amor-phous material with positivity of mucus are very valuableand distinctive features in the accurate diagnosis of this rarevariant of breast carcinoma.

References1. Anderson RJ, Johnston WM, Szpack CA. Fine needle aspiration of

adenoid cystic carcinoma metastatic to the lung: cytologic features anddifferential diagnosis. Acta Cytol 1985;29:527–532.

2. Buchanan AJ, Fauck R, Gupta RK. Cytologic diagnosis of adenoidcystic carcinoma in tracheal wash specimens. Diagn Cytopathol1988;4:130–132.

3. Eneroth CM, Zajicek J. Aspiration biopsy of salivary gland tumours.IV. Morphological studies on smears and histologic sections from 45cases of adenoid cystic carcinoma. Acta Cytol 1969;13:59–63.

4. Frable WG, Gopelrud DG. Adenoid cystic carcinoma of Bartholin’sgland: diagnosis by aspiration biopsy. Acta Cytol 1973;19:152–153.

5. Geisinger KR, Reynolds GD, Vance RP, McGuirt WF. Adenoid cysticcarcinoma arising in a pleomorphic adenoma of the parotid gland: anaspiration cytology and ultrastructural study. Acta Cytol 1985;29:522–526.

6. Grafton WD, Kamm RC, Cowley LH. Cytologic characteristics ofadenoid cystic carcinoma of the cervix uteri. Acta Cytol 1976;20:164–166.

7. Gupta RK, McHutchison AGR. Cytologic findings of adenoid cysticcarcinoma in a tracheal wash specimen. Diagn Cytopathol 1992;8:196–197.

8. Lozowski MS, Mishriki Y, Solitare GB. Cytopathologic features ofadenoid cystic carcinoma. Acta Cytol 1983;27:317–322.

9. Oertel YC, Esteban JM, Quintos EJ. Adenoid cystic carcinoma ofbreast diagnosed by fine needle aspiration (cytology). (exercise no.C83-1). Chicago: ASCP; 1983.

10. Playfker J, Mosher JL. Fine needle aspiration of liver with metastaticadenoid cystic carcinoma. Acta Cytol 1983;27:323–325.

11. Smith RC, Amy RW. Adenoid cystic carcinoma metastatic to the lung:report of a case diagnosed by fine needle aspiration biopsy cytology.Acta Cytol 1985;29:533–534.

12. Galed-Placed I, Garcia-Ureta E. Fine needle aspiration biopsy diagno-sis of adenoid cystic carcinoma of the breast. A case report. Acta Cytol1992;36:364–366.

13. Stanley MW, Tani EM, Rutquist L, Skoog L. Adenoid cystic carcinomaof the breast. Diagnosis by fine-needle aspiration. Diagn Cytopathol1993;9:184–187.

14. Gupta RK, Dowle CS. Fine needle aspiration cytodiagnosis of adenoidcystic carcinoma of the breast. Diagn Cytopathol 1996;14:328–330.

15. Gupta RK, Rao S, Picken G. Needle aspiration cytology of unsuspectedadenoid cystic carcinoma of the hip. J Jpn Soc Clin Cytol 1997;36:541–544.

16. Galloway JR, Woolner RB, Clagett OT. Adenoid cystic carcinoma ofthe breast. Surg Gynecol Obstet 1966;122:1289–1294.

17. Peters GN, Wolff M. Adenoid cystic carcinoma of the breast: report of11 new cases: review of the literature and discussion of biologicalbehaviour. Cancer 1979;1752–1760.

18. Harris M. Pseudoadenoid cystic carcinoma of the breast. Arch PatholLab Med 1977;101:307–309.

19. Highland KE, James LF, James SAN, Silverman JF. Collagenousspherulosis: report of a case with diagnosis by fine needle aspirationbiopsy with immunocytochemical and ultrastructural observations.Acta Cytol 1993;37:3–9.

GUPTA ET AL.

84 Diagnostic Cytopathology, Vol 20, No 2