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Utility of Fine-Needle Aspiration As a Diagnostic Technique in Lymphoma

From the Departments of Medicine and Pathology and the Arizona Cancer Center, University of Arizona, Tucson, AZ

Address reprint requests to Thomas P. Miller, MD, Arizona Cancer Center, 1515 N Campbell Ave, PO Box 245024, Tucson, AZ 85724-5024

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
PURPOSE: To evaluate, from a clinician's perspective, the sensitivity and specificity of fine-needle aspiration (FNA) as a technique for the diagnosis of lymphoma.

PATIENTS AND METHODS: Medical records of 470 new patients seen in one lymphoma specialist's clinic from January 1998 through December 2002 were reviewed. Ninety-nine (21%) of the 470 patients underwent a total of 115 FNA procedures, which were assessed by more than 70 different pathologists in 32 different pathology departments. Subsequent excisional biopsies were performed in 67 of these patients and interpreted by a single hematopathology group without independent review.

RESULTS: Of 115 FNA procedures, 93 were completed for the initial evaluation of lymphoma and 22 were done for assessment of relapsed disease. Of the 93 FNA attempts at initial diagnosis, only 27 (29%) were given a specific and complete histologic diagnosis using an accepted classification system (Working Formulation, Revised European-American Classification of Lymphoid Neoplasms, WHO). For the 22 FNAs done for recurrent disease, only nine (41%) were classified using an accepted system. Sixty-seven (72%) of the 93 FNAs performed for the evaluation of initial disease had subsequent excisional biopsies. Among these paired comparisons, only eight (12%) of 67 FNA diagnoses were correlated with the subsequent excisional biopsy diagnosis. Immunophenotyping was completed on 24 of the 67 paired FNAs. Seven of the 24 FNAs with immunophenotyping (29%) were correlated with subsequent histology on excisional biopsy. Only one (2%) of 43 FNA diagnoses, based on morphology alone, was correlated with subsequent excisional biopsy diagnosis.

CONCLUSION: Overall, FNA for lymphoma diagnosis is not helpful, not cost effective, and in addition may misguide treatment.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
Although fine-needle aspiration (FNA) has been in use for the past century, only in the last 20 years has it been used with any frequency to diagnose lymphomas.^1–3 In fact, FNA is gaining popularity as a diagnostic technique for evaluating lymphomas, with more than 200 articles written on the subject since 1985.⁴ Citations from the 1980s and early 1990s state that the technique is reliable for both confirmation of recurrent disease and for evaluation of disease extent in patients with a history of lymphoma.^5–7 In the late 1990s, the technique became used increasingly for the initial diagnosis of lymphoma. Some current literature asserts that FNA is now the preferred initial diagnostic test for the evaluation of supraclavicular lymphadenopathy.⁸ Multiple articles discuss improved accuracy of diagnosis with the addition of ancillary techniques, such as immunophenotyping, to standard cytologic evaluation.^1,9–14 Since the Revised European-American Classification of Lymphoid Neoplasms (REAL) and the WHO classification systems^15,16 increased reliance on immunophenotyping, some have speculated that the utility of FNA for diagnosis of lymphoma is enhanced further.

Although the use of FNA as a diagnostic technique for both the diagnosis of initial and recurrent lymphoma has increased over the last two decades, it is still considered to be inadequate by many clinicians.¹⁰ In our experience, we have observed an increasing number of patients presenting to the lymphoma clinic who have had FNA as a diagnostic procedure. A review of published studies finds that most reports emphasize the diagnostic utility of FNA, sensitivity/specificity of the procedure, or specific techniques for performing and evaluating FNA. However, an analysis of the clinical utility of FNA, with specific reference to managing lymphoma, is not available.

	PATIENTS AND METHODS

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This is a retrospective chart review of new patients seen by one lymphoma specialist. Records of consecutive patients over a 5-year period from January 1998 through December 2002 were examined. These patients include newly diagnosed individuals as well as referrals sent for second opinions. New patients seen over this time period with diagnoses of lymphoma, non-Hodgkin's lymphoma (NHL), Hodgkin's lymphoma, and lymphadenopathy were included. Patients presenting with diagnoses of chronic lymphocytic leukemia, multiple myeloma, or solid tumors were excluded from the review. Human subjects committee exemption was obtained for the chart review.

The charts were reviewed for the pathologic diagnosis and to determine whether FNA was performed. Those patients who had at least one FNA were identified. They were then categorized based on whether the FNA was done at initial diagnosis or at recurrence. If an excisional biopsy was done in addition to the aspiration, the results of the diagnoses were compared. These excisional biopsies were interpreted by a single hematopathology group without independent review. Additional data obtained included dates of FNA and excisional biopsies, ancillary techniques used (flow cytometry, immunostains, DNA analysis, and so on), examining pathology departments, biopsy sites, and whether treatment decisions were based solely on FNA.

More than 70 pathologists were involved in the interpretation of FNAs. These often included different pathologists for review of morphology versus review of ancillary studies. Thirty-two different pathology centers in 21 cities and 12 states were involved in the diagnostic evaluation. Diagnostic techniques used for the evaluation of FNAs included morphology only (45%) and immunophenotyping in addition to morphology (42%); in 13%, the specific technique used was not recorded.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
Four hundred seventy patients fit the inclusion criteria for this review. Ninety-nine of these patients (21%) underwent a total of 115 FNA procedures (some underwent more than one FNA procedure). Ninety-three of the FNAs were done for initial evaluation of disease, and 22 were done for assessment of relapsed lymphoma. The female to male ratio was nearly one to one, with 51% female and 49% male patients. The age range of the cohort was 19 to 94 years, with a mean age of 53 years. There were 16 different anatomic regions biopsied by FNA. The most frequent site was the neck/cervical area, comprising 38% of the aspirations. The next most frequent were the supraclavicular and retroperitoneal regions, each comprising 9.5% of the total. The complete list of sites biopsied is shown in Table 1.

Initial Diagnoses
Sixty-seven of the 93 FNAs that were completed for the initial evaluation of lymphoma had subsequent excisional biopsies, as shown in detail in Table 3. The 67 aspirations were performed on 60 individuals (some patients had > one FNA procedure). In summary, 12% of the FNA diagnoses were correlated with results from subsequent excisional biopsies. The most common diagnoses by excisional biopsy were follicular lymphomas (33.3%) and diffuse large B-cell lymphomas (DLBCL; 26.7%). By contrast, the most common diagnoses by FNA were atypical/abnormal findings (23.9%), nondiagnostic (20.9%), and lymphoma without subtype (19.4%). Four (20%) of 20 follicular lymphomas were correctly identified by FNA, whereas only one of 16 DLBCLs (6.3%) was correctly identified. Interestingly, no T-cell lymphomas (n = 3) were correctly diagnosed by FNA. Five aspirations, which were diagnosed as negative for malignancy, were eventually recognized to be follicular (n = 2), DLBCL (n = 2), and Burkitt's-like lymphomas (n = 1). One DLBCL diagnosed by excisional biopsy was mistakenly identified as a thymoma by FNA. The remainder of the comparisons are shown in Table 3.

In three of the 93 FNAs, there was disagreement regarding interpretation of FNA results. One patient underwent two FNA procedures, both of which were diagnosed as follicular NHL. On review by a lymphoma specialist, the diagnosis was changed to mucosal-associated lymphoid tissue NHL. The second patient underwent one FNA, which was originally interpreted as an atypical lymph node. This was reviewed later by a lymphoma specialist and the diagnosis was changed to LCL.

Seventeen patients underwent 18 FNAs for initial diagnosis with no confirmatory tissue biopsy. Fifteen of these FNAs yielded a diagnosis with specific lymphoma subtype. One FNA was interpreted as well-differentiated lymphoma, one as suggestive of lymphoma, and one as adenocarcinoma. The later patient underwent a second FNA, which was then interpreted as LCL, not adenocarcinoma.

Recurrent Diagnoses
Only five of the 22 FNAs done for the evaluation of recurrent disease had a subsequent excisional biopsy completed. These five paired FNA-biopsies were performed on three patients. The first patient had an FNA interpreted as benign. However, the excisional biopsy showed follicular NHL. The FNA for the second patient stated malignant neoplasm, whereas the excisional biopsy was more specific in diagnosing DLBCL. The final individual underwent three separate FNA procedures before the eventual excisional biopsy. The first FNA was nondiagnostic, the second was suggestive of lymphoma, and the third gave a diagnosis of Hodgkin's lymphoma. The excisional biopsy result confirmed Hodgkin's lymphoma as the diagnosis.

Sixteen FNAs done on 15 patients for the evaluation of recurrent disease had no subsequent excisional biopsy with which to compare. Results of six of the FNAs were consistent with the patients' historical diagnoses. Three patients with historical diagnoses of NHL were diagnosed as having lymphoma (without mention of subtype) by FNA. Two patients with history of follicular lymphomas were diagnosed with more aggressive disease (high-grade NHL and LCL) by aspiration of recurrent lymph nodes. Two patients with historical diagnoses of low-grade NHL were more appropriately classified as having follicular lymphomas by FNA. Finally, of patients with histories of mucosal-associated lymphoid tissue, follicular, and mantle-cell lymphomas, FNAs evaluated for recurrent disease rendered diagnoses of nondiagnostic, atypical, and benign, respectively.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
From the perspective of a clinician attempting to design a treatment plan for patients with lymphoma, we found FNA to be woefully inadequate. In 67 patients with both FNA and excisional biopsy done at the time of initial diagnosis, we found 12% concordance. An additional 21% were correctly diagnosed using the broader term of lymphoma, without further histologic subtyping. We consider this group as having an inadequate diagnosis for management. Therefore, 88% of patients were given FNA cytology diagnoses that were clinically inadequate on which to base treatment decisions. This group includes those categorized as nondiagnostic, atypical/abnormal lymph node, suggestive of lymphoma or malignancy, and the 21% having the broad diagnostic category of lymphoma. More worrisome is our finding that 15% were given a wrong diagnosis (a specific but incorrect histologic subtype). There were five false-negative samples and one false-positive. In some instances, patients were treated incorrectly based on a faulty diagnosis. These results differ from previous published reports regarding the efficacy of FNA.^1,5,6,9

As mentioned, hundreds of articles have been written regarding this subject, with most of this literature coming from academic institutions. Most studies testing sensitivity of FNA as a diagnostic tool reflect the correlative results of a single university-based pathologist or group. Our study reflects community practice in that FNAs were performed by more than 70 pathologists in 12 different states. Further, in our study, the FNA and excisional biopsy results were independently correlated.

Concern over the use of FNA in the evaluation of lymphoma is recognized in some pathology literature. One article acknowledges that many pathology training programs do not give adequate exposure of diagnostic cytology to trainees, therefore, questioning the usefulness of FNA cytology in the general community practices.¹⁰ An interesting survey examined the practices of a range of community pathologists in relation to how they deal with examination of lymph nodes.¹⁷ Although 80% of community pathologists surveyed feel that FNA yields a diagnosis less than one half of the time, nearly one third of pathologists use FNA the majority of the time.¹⁷ This disparity between the apparent belief in the limited utility and the continued use of the technique is curious.

Although many community pathologists feel that FNA has limited efficacy in the evaluation of lymph nodes and lymphoma, its use is increasing.^4,17 This may, in part, be due to perceived advantages of the procedure. First, FNA is said to be a more rapid and cost-effective procedure than most excisional biopsies.^9,12 Second, FNA may be accomplished by either tactile guidance, computed tomography, or ultrasound guidance, or endoscopic ultrasound in many cases, obviating the need for surgical biopsy.¹⁸ Because of the small puncture site, decreased discomfort, morbidity, and mortality are cited as advantages.^9,11,12 FNA may be used in biopsies of difficult to reach areas such as liver, spleen, abdomen, retroperitoneum, and other sites not easily accessible to surgery.^13,19 FNA is also said to have merit in the extremely ill patients for which a surgical biopsy would be potentially dangerous.⁷

Our results question many of these claims. First, although the FNA procedure itself may take less time than a surgical biopsy, nondiagnostic results necessitate an additional procedure. In our experience, most patients in our review required a second procedure, adding to the cost, discomfort, and delay in treatment. The average time elapsed between inadequate FNA and eventual excisional biopsy diagnosis was more than 35 days. Second, although advocates of FNA claim it to be a safer means of obtaining a diagnosis in difficult to reach areas (liver, retroperitoneum, spleen), only one third of the anatomic sites evaluated in our consecutive case series were considered difficult to access by a surgical procedure, and many of these sites are becoming less difficult to access as minimally invasive procedures are developed.²⁰

Although FNA of lymph nodes is well described, it is reported to be useful in evaluating lymphomas found in other uncommon tissues as well. For example, there are reports in the literature of its use in diagnosis of primary intraocular NHL.^21,22 Lung lesions are claimed to be more safely evaluated by FNA, and this has been used in diagnosis of lymphoma in this uncommon area.²³ Other unusual areas cited in the literature where FNA has been used for the evaluation of lymphoma include thyroid, salivary gland, and breast.^24–27 With the exception of intraocular NHL, all of the other non-nodal sites mentioned were evaluated by FNA in our group of patients. However, of the 12 FNAs completed on lung, breast, thyroid, and salivary glands, only one FNA (8%) yielded a correct diagnosis. The morbidity was not decreased, as all patients eventually underwent an excisional biopsy in addition to the FNA.

Although FNA is said to have certain advantages over open biopsy, certain inherent limitations have been considered. These limitations have generally been classified as loss of architecture (resulting in difficulty differentiating between follicular and diffuse histologies),^28–30 sampling error,^10,17,31 difficulty in distinguishing reactive cells from malignant cells,^30,32 and lack of adequate material (which may not allow for flow cytometry or additional stains).^10,32 These limitations likely were a major cause of the poor performance of FNA seen in our cohort of patients.

There are several specific diseases that are noted to be particularly difficult to assess by FNA. Hodgkin's lymphoma, especially lymphocyte-depleted, are problematic to diagnose by FNA alone because of the paucity of Reed-Sternberg cells and the admixture of nonmalignant cells.^4,28,32–34 T-cell NHL and T-cell rich B-cell lymphoma may be difficult to differentiate from one another as well as Hodgkin's lymphoma using FNA.^7,33,35,36 Grading lymphomas is difficult, at best, and is not enhanced with smaller sample sizes. Partial transformation of follicular to high-grade disease is also compromised with limited tissue. Finally, evaluation of composite lymphomas, marginal-zone lymphomas, Ki-1 anaplastic large-cell NHL, polyclonal posttransplantation lymphoproliferative disorders, and primary mediastinal LCL are each associated with unique difficulties that make diagnosis with FNA difficult, if not impossible.^29,31,37 Our data confirms difficulty assessing these particular diagnoses. None of the patients diagnosed with T-cell lymphoma, T-cell rich B-cell lymphoma, anaplastic LCL, or primary mediastinal LCL were correctly diagnosed by FNA. However, the evaluation of Hodgkin's lymphoma was better than expected, with a 50% accuracy using FNA (although subtype was variably described). Of note, no attempt to grade follicular lymphomas was made by pathologists evaluating FNA cytologies in our patients.

Diagnostic sensitivity of FNA for the diagnosis of lymphoma cited in the literature ranges between 62% to 100%.^{1,5,6,9,23,26,32,38–40} As noted, the sensitivity of FNA in our study was found to be 12%. We note that most prior reports exclude nondiagnostic samples from analysis, thus effectively increasing the sensitivity.³⁸ Prior reports are largely retrospective, whereas our study evaluated a consecutive series of patients.

In some prior studies, positive correlation has been imprecisely defined. Some authors include the diagnosis of suggestive of lymphoma as a positive correlation.^25,27,38 Other studies are more definitive yet still imprecise, using the term lymphoma without mention of subtype^{1,8,10,19,23,32} or low- or high-grade lymphoma^1,5,32,39 or differentiating between B- and T-cell lymphoma²⁷ as examples of FNA accuracy. From a clinician's perspective, these are not sufficient. Some earlier studies did use the Rappaport classification and the Working Formulation.^6,26,40,41 Many of the recent studies use the REAL or WHO classification systems.^1,18,24,42 In our review, 18% of FNAs gave a diagnosis of lymphoma without a specific subtype. To direct appropriate treatment choices, it is necessary to provide a complete diagnosis using subclassification by either REAL or WHO classification systems.

Modern pathology practice commonly applies ancillary techniques, such as flow cytometry or immunocytochemistry, to standard cytologic examination.^11,14,32 Studies have demonstrated improved results with the addition of such techniques.³² This was confirmed by our study. Those FNAs evaluated with immunophenotyping, in addition to morphology, had a significantly better correlation with excisional biopsy than those FNAs evaluated alone (29% v 2%, respectively; P = .002). Although emphasis is placed on the importance of ancillary techniques, these additional tests were used less than 50% of the time by pathologists in our review. For the initial diagnosis of lymphoma, ancillary techniques were used 41% of the time. The use increased only slightly in FNA done for recurrent disease (45%). Immunophenotyping seems to improve results, and inasmuch as immunophenotyping use is increasing, we look forward to possible improvement in diagnosis using FNA cytology.

Although histologic diagnosis of tissue biopsy is the gold standard for evaluation of lymphoma, FNA is increasingly used for both initial and recurrent disease. One fifth of the new patients seen in a lymphoma clinic over a 5-year period had at least one FNA procedure. Although the incidence of FNA use has increased, our study raises serious questions regarding its accuracy and utility.

	Authors' Disclosures of Potential Conflicts of Interest

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
The authors indicated no potential conflicts of interest.

	Acknowledgment

 
We thank Barbara Hauck for her help in preparation of this manuscript.

	NOTES

 
Supported in part by a grant from Rita Golding in memory of Melville Golding.

Preliminary data presented in both poster and abstract form at the 2003 Conference of the American Society of Hematology, San Diego, CA, December 6-9, 2003 (abstract 1436).

Authors' disclosures of potential conflicts of interest are found at the end of this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
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Submitted February 13, 2004; accepted May 6, 2004.

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