41292606 Pitfalls in Salivary Gland FNA

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26 Arch Pathol Lab Med—Vol 129, January 2005 Salivary Gland Fine-Needle Aspiration Cytology —Hughes et al

Pitfalls in Salivary Gland Fine-NeedleAspiration Cytology

Lessons From the College of American Pathologists Interlaboratory ComparisonProgram in Nongynecologic Cytology

Jonathan H. Hughes, MD, PhD; Emily E. Volk, MD; David C. Wilbur, MD; for the Cytopathology Resource Committee, College of American Pathologists

● Context.—We use data from the College of American Pa-thologists Interlaboratory Comparison Program in Nongy-necologic Cytology to identify common diagnostic errorsin salivary gland fine-needle aspiration (FNA).

Objective.—To identify salivary gland FNA cases withpoor performance characteristics in the NongynecologicCytology Program surveys, so that the most common di-agnostic pitfalls can be avoided.

Design.—A retrospective review of the College of Amer-ican Pathologists Nongynecologic Cytology Program’s cu-mulative data from 1999 to 2003 revealed the most com-mon false-positive and false-negative interpretations onFNA for common salivary gland lesions. Slides that per-formed poorly were then reviewed to identify the cytologiccharacteristics that may have contributed to their poorperformance.

Results.—A total of 6249 participant responses with gen-eral interpretations of benign (n 4642) or malignant (n

1607) were reviewed. The sensitivity and specificity of the

participant responses for correctly interpreting the casesas benign or malignant were 73% and 91%, respectively.Benign cases with the highest false-positive rates were

monomorphic adenoma (53% false-positive), intraparotidlymph node (36%), oncocytoma (18%), and granuloma-tous sialadenitis (10%). Malignant cases with the highestfalse-negative rates were lymphoma (57%), acinic cell car-cinoma (49%), low-grade mucoepidermoid carcinoma(43%), and adenoid cystic carcinoma (33%). Selected re-view of the most discordant individual cases revealed pos-sible explanations for some of the interpretative errors.

Conclusions.—These data confirm the difficulty associ-ated with interpretation of salivary gland FNA specimens.Cytologists should be aware of the potential false-positiveand false-negative interpretations that can occur in FNAsfrom this organ site in order to minimize the possibility of diagnostic errors.

(Arch Pathol Lab Med. 2005;129:26–31)

The Interlaboratory Comparison Program in Nongyne-cologic Cytopathology (NGC) was inaugurated by the

College of American Pathologists (CAP) in 1997. Most par-ticipating laboratories are in the United States, although asmall number of international laboratories also subscribe.Participating NGC Program laboratories receive quarterlymailings of 5 glass slides with accompanying clinical his-tories. The slides are contributed to the program by members of the CAP Cytopathology Resource Committee andare reviewed at several screening sessions for consensusprior to inclusion in the program. All of the Cytopathol-ogy Resource Committee pathologists are certified by the

American Board of Pathology and hold subspecialty cer-tification in cytopathology. Many, if not most, of the Cy-

Accepted for publication September 9, 2004.From Laboratory Medicine Consultants, Ltd, Las Vegas, Nev (Dr

Hughes); the Department of Pathology, William Beaumont Hospital,Troy, Mich (Dr Volk); and the Department of Pathology, MassachusettsGeneral Hospital, Boston (Dr Wilbur).

The authors have no relevant financial interest in the products orcompanies described in this article.

Reprints: Jonathan H. Hughes, MD, PhD, Laboratory Medicine Con-sultants, Ltd, 3059 S Maryland Pkwy, #100, Las Vegas, NV 89109-2201(e-mail: [email protected]).

topathology Resource Committee members are nationallyand internationally recognized experts in fine-needle as-piration (FNA) cytology. Submitted cases must be vali-dated by 2 Cytopathology Resource Committee cytopa-thologists, who agree on the general and specific interpre-tation and who also agree that the slide is representativeand has no technical inadequacies that might inhibit anaccurate assessment. An interpretative menu that uses a bubble answer format is provided to the participating lab-oratories with the glass slides. The participants’ responsesare tabulated by the CAP, which then provides a list of thereference diagnoses to the participating laboratories for

education and self-assessment. Individual participants usethe CAP NGC Program as an educational tool as well asa measure of their performance as compared with otherlaboratories. However, because slides circulate extensively,most slides have a unique accrued slide profile, allowingevaluation of the characteristics of each slide in the pro-gram.

The data generated by the NGC survey provide a valu-able source of information about which types of cases pre-sent the most challenging interpretation problems for cy-tologists from a wide range of practice settings. In thisstudy, we used data from the NGC Program to examine



Arch Pathol Lab Med—Vol 129, January 2005 Salivary Gland Fine-Needle Aspiration Cytology —Hughes et al 27

Table 1. Reference Diagnoses Available toNongynecologic Cytology Program Participants forSalivary Gland Fine-Needle Aspiration Specimens*

Reference Diagnoses

Acinic cell carcinomaAdenocarcinoma, NOSAdenoid cystic carcinomaBenign neoplasm, NOSCyst, NOSLymphoepithelial lesion/cyst

LymphomaMetastatic carcinoma, NOSMetastatic melanomaMonomorphic adenomaMucoepidermoid carcinoma, high gradeMucoepidermoid carcinoma, low gradeNormal salivary gland/sialadenosisOncocytomaPapillary carcinomaPleomorphic adenomaSialadenitis/granulomasSmall cell undifferentiated carcinomaSpindle cell sarcoma, NOSSquamous cell carcinomaUndifferentiated carcinomaUnsatisfactoryWarthin tumor

* NOS indicates not otherwise specified.

Table 2. Cumulative 1999–2003 Performance Characteristics of the Nongynecologic Cytology Program Respondents’Diagnoses for Common Benign Salivary Gland Lesions

Reference Diagnosis

LaboratoryResponses,

No.

LaboratoryResponses

With CorrectGeneral

Diagnosis:‘‘True-

Negatives’’No. (%)

LaboratoryResponses

With CorrectReferenceDiagnosis,

No. (%)

LaboratoryResponses

With IncorrectGeneral

Diagnosis:‘‘False-

Positives,’’No. (%)

Most CommonFalse-Positive Diagnoses*

Normal salivary gland/sial-adenosis

276 270 (98) 222 (80) 6 (2) Acinic cell carcinoma

Granulomatous sialadenitis 227 204 (90) 116 (51) 23 (10) Adenocarcinoma NOS, lymphomaPleomorphic adenoma 2572 2351 (91) 2109 (82) 221 (9) Adenoid cystic carcinoma, acinic cell

carcinoma, low- and high-grade mu-coepidermoid carcinoma

Warthin tumor 1519 1397 (92) 1077 (71) 122 (8) Lymphoma, acinic cell carcinoma, high-grade mucoepidermoid carcinoma

Monomorphic adenoma 15 7 (47) 1 (7) 8 (53) Adenoid cystic carcinomaOncocytoma 22 18 (82) 3 (14) 4 (18) Acinic cell carcinomaIntraparotid lymph node 11 7 (64) 3 (27) 4 (36) Lymphoma

Total 4642 4254 (91) 3531 (76) 388 (8)


the accuracy of FNA interpretation for salivary gland le-sions and to determine the most common sources of er-rors.

MATERIALS AND METHODS

Cumulative histories of all NGC Program participant respons-es for all salivary gland FNA cases from 1999 through 2003 wereobtained through the CAP’s ‘‘Scores’’ computer system. The caseswere divided into general and reference diagnostic categories forcomparison within category. The general categories were nega-tive, positive, suspicious for malignancy, and unsatisfactory. Thereference diagnoses available to participants are listed in Table 1.

In the first part of the study, the year-end data compiled forall of the reference interpretations were reviewed, and the overallaccuracy, false-positive, and false-negative rates of the NGC Pro-

gram participants were calculated. For the purposes of determin-ing false-positive and false-negative rates, participant responsesof ‘‘suspicious for malignancy’’ were considered ‘‘positive formalignancy.’’ The most common interpretational errors were alsotabulated.

In the second part of the study, data from the Scores systemwere used to identify individual slides that had a high level ofdiscordance between the reference interpretation and the NGCProgram participants’ responses. Although many of these slideshad not circulated enough times to permit rigorous statisticalevaluation of their performance characteristics, many of them

showed consistent, reproducible errors that made their analysisa potential source of information for identifying common pitfalls.A selective review of these slides was undertaken by 2 of theauthors (J.H.H., D.C.W.), and an effort was made to determinethe most likely causes for the interpretation errors.

RESULTS

The results of the 1999–2003 retrospective compilationof NGC Program participants’ responses for salivarygland FNA diagnostic categories are presented in Tables2 and 3.

Table 2 shows the tabulated responses for the slideswith an established general diagnosis of benign. Therewere a total of 4642 responses, 4254 of which carried acorrect general interpretation of benign, resulting in aspecificity of 91%. Three hundred eighty-eight of the caseswere incorrectly interpreted as malignant, resulting in afalse-positive rate of 8%. The highest false-positive rateswere seen in cases of monomorphic adenoma (53% false-positive rate), intraparotid lymph node (36%), oncocyto-ma (18%), and granulomatous sialadenitis (10%). Pleo-morphic adenoma and Warthin tumor, which constitutedthe large majority of the benign cases, were associatedwith false-positive rates of 8% to 9%. The most commonfalse-positive interpretation for pleomorphic adenoma wasadenoid cystic carcinoma, and the most common false-positive interpretation for Warthin tumor was lymphoma.The overall accuracy of the CAP NGC Program partici-pants for making the correct specific reference interpre-

tation was 76%.Table 3 shows the tabulated responses for the slideswith an established general interpretation of malignant.




Table 3. Cumulative 1999–2003 Performance Characteristics of the Nongynecologic Cytology Program Respondents’Diagnoses for Common Malignant Salivary Gland Lesions

Reference Diagnosis*

LaboratoryResponses,

No.

LaboratoryResponses

With CorrectGeneral

Diagnosis:‘‘True-

Positives,’’

No. (%)

LaboratoryResponses

With CorrectReferenceDiagnosis,

No. (%)

LaboratoryResponses

WithIncorrectGeneral

Diagnosis:‘‘False-

Negatives,’’

No. (%)

Most Common

False-Negative DiagnosesAdenoid cystic carcinoma 300 202 (67) 112 (37) 98 (33) Pleomorphic adenoma, monomorphic

adenomaAcinic cell carcinoma 261 132 (50) 103 (39) 129 (49) Normal salivary gland, sialadenosis,

Warthins tumorMucoepidermoid carcinoma, low grade 30 17 (57) 6 (20) 13 (43) Benign cystMucoepidermoid carcinoma, high grade 93 77 (83) 28 (30) 16 (17) OncocytomaAdenocarcinoma, NOS/poly- or mono-

morphic variant238 205 (85) 123 (51) 33 (14) Pleomorphic adenoma

Undifferentiated carcinoma 69 58 (84) 35 (51) 11 (16) No clear patternMetastatic carcinoma, NOS 88 78 (89) 35 (40) 9 (10) SialadenitisSquamous cell carcinoma 33 28 (88) 20 (62) 5 (16) Warthins tumorLymphoma 442 247 (72) 236 (69) 195 (57) Benign lymph nodeSmall cell undifferentiated carcinoma 14 12 (86) 0 2 (14) LymphomaMetastatic melanoma 40 40 (100) 23 (58) 0 (0) None

Total 1607 1096 (68) 721 (48) 511 (32)


There were a total of 1607 responses, 1096 of which car-ried a correct general diagnosis of malignant, resulting ina sensitivity of 68%. Five hundred eleven cases were in-correctly diagnosed as benign, resulting in a false-nega-tive rate of 32%. The highest false-negative rates were seenin cases of lymphoma (57% false-negative rate), acinic cellcarcinoma (49%), low-grade mucoepidermoid carcinoma(43%), and adenoid cystic carcinoma (33%). The overallaccuracy of the CAP NGC Program participants for mak-ing the correct specific reference interpretation was 48%.

The second part of the study involved the selective re-

view of individual cases that showed a high degree ofdiscordance between the reference diagnosis and the NGCProgram participants’ interpretations. Most of these caseshad not circulated enough to generate sufficient partici-pant responses for meaningful statistical analysis of theirperformance, but they were identified by the Scores sys-tem as highly discordant cases. Because these highly dis-cordant cases represented a unique subset of cases thatmight allow insight into potential interpretative pitfalls,they were reviewed in an effort to identify the possiblesources of the errors. Some of these cases were found todemonstrate low cellularity or poor stain quality, andthese factors probably contributed to their poor perfor-mance. However, other discordant cases had good cellu-

larity and were technically adequate. Some examples ofthese latter cases are shown in Figures 1 and 2.Figure 1, A, shows a Diff-Quik–stained case of pleo-

morphic adenoma, incorrectly interpreted as acinic cellcarcinoma. In our analysis of this case, we concluded thatthe most likely reason for this diagnostic error was thefailure to recognize the stromal component of the pleo-morphic adenoma, which was not very prominent in thiscase. The scantness of the stroma, when coupled with fo-cal areas of pseudo-acinar architecture, probably contrib-uted to the poor performance of this case. Had the stromalcomponent been identified, confusion with acinic cell car-

cinoma would be unlikely, given the bland cytologic fea-tures of the cells.

Figure 1, B, shows a Papanicolaou-stained case of aciniccell carcinoma, incorrectly diagnosed as normal salivarygland. Upon reviewing this case, we felt that the mostlikely reason for this error was the failure to appreciatethe cellularity of the lesion, which was greater than thattypically seen in nonneoplastic processes. Additionally,some participants may not have appreciated the architec-ture of the acinar structures, which were more disorga-nized and discohesive than those of normal salivary

gland.Figure 1, C, shows a Papanicolaou-stained case of ade-

noid cystic carcinoma, incorrectly interpreted as lympho-ma by some respondents. This error almost certainly re-sulted from failure to recognize the stromal component ofthe adenoid cystic carcinoma. Had the stroma been ap-preciated, it is unlikely that a diagnosis of lymphomawould have been entertained. However, it is easy to seehow failure to recognize the stroma, when coupled withthe bland monomorphic cytology of the cells, could leadto the incorrect impression of an atypical lymphoprolif-erative process.

Figure 1, D, shows a Papanicolaou-stained case of War-thin tumor, incorrectly interpreted as lymphoma. This is

a well-recognized pitfall that usually results from failureto recognize the oncocytic component of the tumor, par-ticularly in cases in which the lymphoid component pre-dominates.

Figure 1, E, shows a Papanicolaou-stained case of ade-noid cystic carcinoma, incorrectly interpreted as mono-morphic adenoma. Again, this error probably reflects fail-ure to recognize the stromal component of adenoid cysticcarcinoma on the Papanicolaou stain. The false-negativediagnosis of adenoid cystic carcinoma may also be avoid-ed by careful attention to the nuclear features of the tu-mor; the presence of visible nucleoli and any abnormality




Figure 1. Examples of problematic cases. A, Case of pleomorphic adenoma incorrectly diagnosed as acinic cell carcinoma by several Nongy-necologic Cytology Program participants (Papanicolaou stain, original magnification 200). B, Case of acinic cell carcinoma incorrectly diagnosed as normal salivary gland (Papanicolaou stain, original magnification 200). C, Case of adenoid cystic carcinoma incorrectly diagnosed as lym-phoma (Papanicolaou stain, original magnification 200). D, Case of Warthin tumor incorrectly diagnosed as lymphoma (Papanicolaou stain,original magnification 200). E, Case of adenoid cystic carcinoma incorrectly diagnosed as monomorphic adenoma (Papanicolaou stain, original magnification 200). F, Case of metastatic small cell carcinoma incorrectly diagnosed as lymphoma (Papanicolaou stain, original magnification400).

of the chromatin favor a diagnosis of adenoid cystic car-cinoma over monomorphic adenoma, although these help-ful cytologic features are not present in every case.

Figure 1, F, shows a Papanicolaou-stained case of met-astatic small cell carcinoma, incorrectly interpreted aslymphoma. This is another well-described pitfall, but itmight have been avoided in this case by recognizing theabsence of lymphoglandular bodies.

Figure 2, A, shows a case of mucoepidermoid carcinomathat was incorrectly interpreted as Warthin tumor. It is

likely that the abundant dirty background material, whichis commonly seen in Warthin tumor, and the eosinophilictumor cells, which may have been misinterpreted as on-cocytes, led to this error in classification.

Figure 2, B, shows a case of oncocytoma that was in-correctly interpreted as pleomorphic adenoma by all re-spondents. This interpretative error may have been the re-sult of mistaking the vascularity of the oncocytoma for thestranded stroma of pleomorphic adenoma.

Figure 2, C, shows a case of reactive lymphoid hyper-




Figure 2. Examples of problematic cases. A, Case of mucoepidermoid carcinoma incorrectly interpreted as Warthin tumor (Papanicolaou stain,original magnification 200). B, Case of oncocytoma incorrectly interpreted as pleomorphic adenoma (Papanicolaou stain, original magnification200). C, Case of reactive intraparotid lymph node incorrectly interpreted as lymphoma (Diff-Quik stain, original magnification 400). D, Case of pleomorphic adenoma incorrectly interpreted as mucoepidermoid carcinoma (Papanicolaou stain, original magnification 100).

plasia in an intraparotid lymph node that was incorrectlyinterpreted as lymphoma by the majority of respondents.

Although low-grade lymphoma enters the differential di-agnosis of any reactive process, the polymorphous popu-lation of lymphocytes in this case favors a benign process.This problematic case also underscores the importance ofancillary immunophenotyping studies in the evaluation ofany cytologically suspicious lymph node. Participants inthe NGC Program were not supplied with immunophe-notyping results on this case, but such studies would cer-tainly have been useful in excluding a low-grade lympho-proliferative disorder.

Figure 2, D, shows a case of pleomorphic adenoma thatNGC Program participants incorrectly interpreted as low-grade mucoepidermoid carcinoma. In this case, it is likelythat the stroma of the pleomorphic adenoma may have

been misinterpreted as mucin, thereby leading to the er-roneous conclusion that this lesion represents a low-grademucoepidermoid carcinoma.

COMMENT

Salivary gland FNAs are a common specimen in mostpathology practices and present difficult interpretationchallenges. Several large published series have document-ed the accuracy and limitations of salivary gland FNA.The overall accuracy has been reported to be 87% to 100%in distinguishing benign from malignant lesions; FNAalso has a reported sensitivity of 87% to 100% and a spec-

ificity of 90% to 100%.1–8 Most of these series have beengenerated at large academic centers. To our knowledge,

our study is unique in that the CAP NGC Program as-sesses salivary gland FNA accuracy across a diverse groupof practicing pathologists, including academic centers,commercial laboratories, and large and small private prac-tice settings; therefore, these data may more accurately re-flect the diversity of practice conditions. Moreover, be-cause the same slides circulate among numerous partici-pants, the participants’ responses can be tabulated andused to identify particularly problematic individual casesthat provide insight into common diagnostic dilemmasand pitfalls.

Our 5-year review of NGC survey results revealed a73% sensitivity for making the correct general diagnosisof malignant, a 91% specificity for making the correct gen-

eral diagnosis of benign, and an overall diagnostic accu-racy of 48% for making the correct specific reference di-agnosis. These data are similar to those observed in thereported large academic series. The benign lesions thatwere most often misdiagnosed as malignant were mono-morphic adenoma (53% false-positive rate), intraparotidlymph node (36%), oncocytoma (18%), and granulomatoussialadenitis (10%). The malignant lesions that were mostoften misdiagnosed as benign were lymphoma (57%),acinic cell carcinoma (49%), low-grade mucoepidermoidcarcinoma (43%), and adenoid cystic carcinoma (33%).

Our selected review of the most discordant cases pro-




vided some insight into the sources of possible interpre-tation errors. Some of the discordant cases representedwell-described diagnostic pitfalls, such as the false-nega-tive interpretation of acinic cell carcinoma as normal sal-ivary gland9 or the false-positive interpretation of Warthintumor as lymphoma.10 However, some of the most discor-dant cases were not expected. Although we can only spec-ulate as to the reason why some well-validated, technicallyexcellent slides did not perform well, some of the exam-ples of discordant cases depicted in Figure 1 suggest thatfailure to recognize the diagnostically helpful stromalcomponent on Papanicolaou-stained slides may have beenan important factor. This interpretation underscores theimportance of using both a Romanowsky-type stain (suchas Diff-Quik) and the Papanicolaou stain when examiningFNA material from salivary gland, because stromal com-ponents may be more readily identified on the Roma-nowsky stain. Many of the false-positive and false-nega-tive interpretations of lymphoma probably resulted fromthe lack of any accompanying flow cytometry immuno-phenotyping data with the cases. The poor performanceof these cases highlights the importance of immunophe-notyping studies to the interpretation of lymphoid lesions,particularly low-grade lymphoproliferative processes.

Using a 5-year cumulative slide history from the CAPNGC database, we examined the diagnostic accuracy ofthe NGC Program participants for salivary gland FNA.This review included 6249 responses for a wide variety of benign and malignant salivary gland lesions. The datafrom our review demonstrated that salivary gland FNA is73% sensitive and 91% specific for distinguishing between benign and malignant lesions. The overall accuracy ofFNA for correctly identifying the correct specific referenceinterpretation was 48%. Slide review from cases of highdiscordance suggested that some recurrent interpretationsmight be the result of technically suboptimal slides.Among the technically adequate slides, some of the mostdiscordant slides represented classic diagnostic pitfalls,11–19

such as acinic cell carcinoma versus normal salivarygland, lymphoma versus Warthin tumor, and adenoid cys-tic carcinoma versus monomorphic adenoma. Some dis-cordant cases appeared to occur as a result of participants’not recognizing the stromal component of pleomorphicadenoma or adenoid cystic carcinoma on Papanicolaou-stained slides; these cases underscored the importance ofusing a Romanowsky-type stain, which is superior to thePapanicolaou stain for assessing stromal elements, on sal-

ivary gland FNAs. The study also demonstrated the im-portance of ancillary immunophenotyping studies forclassifying lymphoid lesions. Awareness of some of thesepitfalls and application of classic criteria may help im-prove performance characteristics of salivary gland FNAspecimens in the CAP NGC and in daily practice.

We thank Jennifer Haja, College of American Pathologists Non-gynecologic Cytology Program committee staff member, for herhelp with data procurement and slide handling.

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41292606 Pitfalls in Salivary Gland FNA