0001-5547/07/5106-0837/$19.00/0 © The International Academy of Cytology ACTA CYTOLOGICA 837

FINE NEEDLE ASPIRATION

ACTACYTOLOGICA

The Journal ofClinical Cytologyand Cytopathology

Objective

To compare percutaneous and endoscopic ultrasound(EUS)-guided biopsy techniques.

Study Design

From July 2005 to February 2006, all patients referred forEUS-guided fine needle aspi-ration (FNA) were consid-ered. If inclusion criteria weremet, the first 2 biopsy passeswere performed without suc-tion (fine needle capillary[FNC] sampling). Two addi-tional passes were performedusing the same needle with 10mL of applied suction (FNA).A single blinded pathologistlater retrospectively evaluated each set of slides. Fifty-threepatients met inclusion criteria. The study group comprisedpancreatic masses (23), lymph nodes (26), subepithelial

masses (3) and liver lesion (1). There were 38 malignantand 15 benign lesions.

Results

No statistically significant differences were found with thescoring systems considered in the study. In the subgroups of

patients with pancreatic mass-es, lymph nodes, benign diseaseand malignant disease, no sta-tistically significant outcomeswere noted.

Conclusions

No difference exists betweenquality and diagnostic accura-cy of specimens obtained fromEUS-guided tissue acquisition

via FNC and FNA. The decision to use FNC or FNAshould be left to the discretion of the individual endosonog-rapher. (Acta Cytol 2007;51:837–842)

We recommend that the decisionto use FNC sampling or FNA in

EUS-guided biopsy of solid lesionscan be left to the discretion of the

individual endosonographer.

Evaluation of Fine Needle Aspiration vs. FineNeedle Capillary Sampling on SpecimenQuality and Diagnostic Accuracy in EndoscopicUltrasound–Guided Biopsy

Ian Michael Storch, D.O., Daniel Andrew Sussman, M.D., Merce Jorda, M.D., Ph.D.,and Afonso Ribeiro, M.D.

From the University of Miami Hospital and Clinics, Sylvester Comprehensive Cancer Center, Leonard Miller School of Medicine, Miami,Florida, U.S.A.

Drs. Storch and Sussman are Fellows, Division of Gastroenterology.

Dr. Jorda is Associate Professor of Pathology, Department of Surgical Pathology.

Dr. Ribeiro is Assistant Professor of Clinical Medicine, Division of Gastroenterology.

Address correspondence to: Afonso Ribeiro, M.D., Division of Gastroenterology, University of Miami, P.O. Box 016960, Miami, Florida33101, U.S.A. (aribeiro@med.miami.edu).

Financial Disclosure: The authors have no connection to any companies or products mentioned in this article.

Received for publication October 26, 2006.

Accepted for publication January 10, 2007.

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Keywords: aspiration, fine needle; capillary sampling,fine needle; ultrasound, endoscopic.

During endoscopic ultrasound–guided fine needleaspiration (EUS-FNA) biopsy, it has been sug-

gested that sample adequacy decreases from 100% to71% when no onsite cytopathologist or cytotechnolo-gist is present.1 However, at many institutions, time,personnel and financial considerations limit the avail-ability of these services. In this environment, utiliza-tion of biopsy techniques that minimize backgroundblood while maximizing specimen quality is desirable.

Two biopsy techniques have been described to ob-tain cytology samples using a fine needle.2 The firstmethod, fine needle capillary (FNC) sampling, entailsplacing a hollow needle within a lesion, removing thestylet and moving it back and forth, which allows thecapillary action of the cylindrical needle to draw sam-ple into the chamber without applying an externalforce. Proponents of FNC sampling have claimed thatit yields a small quantity sample with high diagnosticyield because of a decreased amount of sanguineousstaining. The alternative method, FNA, uses a syringeto produce a negative pressure within the needlechamber. This technique was introduced in the 1960sto address the problem of failed FNC sampling biop-sy (specifically in sclerotic tumors, deeply placedskeletal lesions and small mobile lumps). AlthoughFNA is more traumatic than FNC, it is thought to in-crease the amount of tissue obtained.3 FNA is cur-rently the standard biopsy technique used with endo-scopic ultrasound (EUS) at most institutions, with fewendosonographers using FNC sampling as a primarymodality.4

Comparisons of FNA and FNC sampling have beenperformed in percutaneous biopsy with conflicting re-sults.5-14 The present study was performed to directlycompare specimen quality of FNC and FNA samplingtechniques in EUS-guided needle biopsy of a hetero-geneous group of solid lesions.

Methods and Materials

This study is a retrospective, cytopathologist-blindedreview of consecutive patients referred to a tertiary ac-ademic center for EUS-guided biopsy of solid lesions≥ 10 mm maximum cross-sectional diameter from July2005 through February 2006. All EUS studies wereperformed as the primary diagnostic tool for solidmass lesions identified on prior imaging. Patients wereexcluded from the study if they had severe coagulopa-thy (international normalized ratio [INR] ≥ 2) or ifthere was a physical impediment to biopsy such as avascular structure obstructing the path of the biopsyneedle. Patients were also not included if they weredifficult to sedate, as the increased time for biopsy by

the 2 techniques may have endangered patient safety.Procedures were performed in the endoscopy unit ofthe University of Miami Hospital and Clinics inMiami, Florida. Informed consent was obtained fromall patients before the procedure. Collection of datafor this study was approved by our institution reviewboard (IRB protocol number 20060046).

EUS was performed using the linear array echoen-doscope (GF-UC140P; Olympus America Corpora-tion, Melville, New York, U.S.A.) under titrated in-travenous conscious sedation (using meperidine andmidazolam). All lesions had an endosonographic ap-pearance of solid lesions. No cystic-solid lesions wereincluded in the study. If > 1 lesion (i.e., a mass and alymph node) was found in an individual patient, onlythe first lesion sampled was included in the study. Tominimize sampling error, the FNA needle was passedthrough the largest diameter possible in each lesion.Two needle passes using a 22-gauge needle (Echotip;Wilson-Cook, Winston-Salem, North Carolina,U.S.A.) were first performed without using suction(FNC sampling). With each pass of the needle, 10 ex-tension and retraction cycles were repeated. Aftereach pass, the cytologic specimens were placed on 2glass slides and fixed in absolute alcohol solution forstaining. The FNC sampling slides obtained wereplaced into a cassette and labeled as “A.” The needlewas then washed vigorously with 20 mL of normalsaline, and 2 additional passes were performed with 10cc of suction pressure applied to the needle with astandard syringe (FNA). The slides were prepared in asimilar manner and placed in a separate cassette andlabeled as “B.” Additional passes were made at the dis-cretion of the endosonographer for at least 4 totalpasses into lymph nodes, subepithelial lesions andliver lesions, as well as 7 total passes into pancreaticmasses. These additional slides were placed in a cas-sette and labeled as “C” and were not included in thedata analysis of FNC and FNA. No onsite cytopathol-ogy was used for slide review.

Cytologic samples were retrospectively reviewed byan experienced cytopathologist for adequacy, final di-agnosis and scoring using the scoring system de-scribed by Mair et al5 and a modified version of thissystem described by Kulkarni et al18 after each groupof 10 patients was enrolled. The system described byMair et al is a categorical, ordinal scale (scores of 0, 1and 2) that is used to evaluate cytopathology slides ineach of the following areas: background of blood orclot, amount of cellular material, degree of cellular de-generation, degree of cellular trauma and retention ofappropriate architecture (total score of 0–10) (TableI). Cellular degeneration was defined as cellularchanges related to cell death and necrosis. Cellulartrauma was defined as artifact from the tissue prepara-

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tion process due in large part to crush artifact. Themodified scoring system described by Kulkarni et al18

(range, 5–20) is an exponential scale with a base 2 de-rived from the score used by Mair et al.5 For example,if a patient has a score in the system described by Mairet al of 0, 1, 2, 2 and 1 (total 6), the modified scorewould be 1, 2, 4, 4 and 2 (total 13). The exponentialscale may allow a better discrimination among middlescores and may improve discrimination of “average”quality cytology slides. In this study, the cytopatholo-gist was aware of the lesion source (lymph node, pan-creatic mass or submucosal lesion) but blinded to thefinal diagnosis or method used for sampling in eachslide set (FNA or FNC sampling).

A positive diagnosis of malignancy was considered atrue positive. In all other cases, further diagnostic pro-cedures, clinical course and imaging studies were usedto establish or exclude malignancy.

The primary endpoint was specimen quality and di-agnostic accuracy of FNC sampling and FNA as as-sessed by the modified score described by Kulkarni etal.18 Secondary endpoints included diagnostic yield,score described by Mair et al5 and modified scoreamong subgroups of pancreatic masses, lymph nodes,benign lesions and malignant lesions.

Statistical Analysis

Statistical tools from the worldwide web pagewww.statspage.org were used to perform descriptiveanalyses. Differences in the score described by Mair etal5 and modified score (cardinal, ordinal variables)were tested by the paired t test for comparison of FNCsampling and FNA sampling techniques as well as sub-group analyses. For all statistical analyses, results wereconsidered statistically significant at an α level of 0.05.

Results

A total of 53 procedures were performed on 53 pa-tients (Table II). There were 33 men and 20 womenwith a mean age of 66 years (range, 38–89). Therewere 38 patients with malignant processes and 15 withbenign diseases. The following lesions were sampled:pancreatic tumors (23), lymph node (26), subepitheliallesions (3) and liver lesion (1). The mean size of lesionssampled was 29 mm (range, 10–50 mm). Thirty-fivepatients had large lesions (> 25 mm) and 18 had smalllesions (≤ 25 mm). All patients had 2 FNC and 2 FNAneedle passes and additional passes were done at thediscretion of the endosonographer for at least 7 pass-es in pancreatic masses and 4 in lymph nodes, subepi-thelial lesions and hepatic lesions. The mean numberof total needle passes was 6.9 (range, 4–10). The accu-racy of EUS-guided biopsy to differentiate malignantfrom benign disease was 92.4% (49 of 53) consideringall needle passes. If only the initial 4 passes (FNC sam-

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Table I Score Described by Mair et al5

Criterion Description Score

Background blood or clot Large amount; great compromise to diagnosis 0

Moderate amount; diagnosis not possible 1

Minimal; diagnosis easy; specimen “textbook” quality 2

Amount of cellular material Minimal to absent; diagnosis not possible 0

Sufficient for cytodiagnosis 1

Abundant; diagnosis simple 2

Degree of cellular degeneration Marked; diagnosis impossible 0

Moderate; diagnosis possible 1

Minimal; good preservation; diagnosis easy 2

Degree of cellular trauma Marked; diagnosis not possible 0

Moderate; diagnosis possible 1

Minimal; diagnosis obvious 2

Retention of appropriate architecture Minimal to absent; nondiagnostic 0

Moderate; some preservation 1

Excellent; diagnosis obvious 2

Table II Demographics

Lesion data Factor No.

Total patients 53

Mean age (range) 66 (38–89)

Gender 33 M:20 F

Lesion source Pancreatic masses 23

Lymph nodes 26

Subepithelial masses 3

Liver 1

Benign vs. malignant Benign disease 15

Malignant disease 38

Lesion size (mm) Mean 29

Range 10–50

Number > 25 mm 35

Number ≤ 25 mm 18

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pling and FNA) for the study were considered, the ac-curacy was 73.5% (39 of 53). There was no statisticaldifference between FNC sampling and FNA in any ofthe variables analyzed (Table III). The scores de-scribed by Mair et al5 for FNC sampling and FNAwere, respectively, 4.00 and 3.37 (p = 0.28), and themodified scores for FNC sampling and FNA were, re-spectively, 11.8 and 10.9 (p = 0.44).

Subgroup analysis of pancreatic masses, lymphnodes and benign and malignant disease showed nostatistical difference in the Mair score or modifiedscore (Table III). The mean Mair score for benign le-sions with FNC sampling and FNA was 3.50 and 2.61,respectively (p = 0.38). The mean Mair score for ma-lignant lesions with FNC sampling was 4.27 and withFNA was 3.79 (p = 0.49). The mean modified Mairscore for benign lesions with FNC sampling and FNA

was 10.7 and 9.28, respectively (p = 0.45). The meanmodified Mair score for malignant lesions with FNCsampling was 12.4 and with FNA was 11.8 (p = 0.69).No statistical significance was observed between be-nign and malignant lesions with respect to mean FNCsampling Mair score (p = 0.39), mean FNA Mair score(p = 0.15), mean FNC sampling modified Mair score(p = 0.32) or mean FNA modified Mair score(p = 0.10).

Overall, larger lesions (> 25 mm) had a statisticallysignificant higher Mair score and modified Mair scorein both FNA and FNC sampling compared to smallerlesions (≤ 25 mm). However, FNC and FNA them-selves were similar when sampling a large or a small le-sion (Mair and modified Mair score; Table III). Therewere no complications from EUS-guided biopsy andno adverse events in this study.

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Table III Results

Measure Mean FNC Sampling Score Mean FNA Score p

Background blood (0–2) 1 0.96 0.64

Cellular material (0–2) 0.9 0.77 0.43

Cellular degeneration (0–2) 0.98 0.85 0.44

Cellular trauma (0–2) 0.96 0.9 0.75

Architecture (0–2) 0.94 0.88 0.74

Mair score (0–10) 4.00 3.37 0.28

Modified Mair score (5–20) 11.76 10.92 0.44

Mean FNC Mair Score Mean FNA Mair Score

Pancreatic masses 5.04 4.91 0.9

Lymph nodes 5.19 3.96 0.25

Benign disease 3.50 2.61 0.38

Malignant disease 4.27 3.79 0.49

Small lesion (≤ 25 mm) 3.50 2.83 0.51

Large lesion (> 25 mm) 5.57 5.17 0.67

Mean FNC Sampling Mean modified

modified Mair Score FNA Mair Score

Pancreatic masses 11.9 11.7 0.89

Lymph nodes 11.9 10.3 0.32

Benign disease 10.7 9.28 0.45

Malignant disease 12.4 11.8 0.69

Small lesion (≤ 25 mm) 9.28 8.5 0.57

Large lesion (> 25 mm) 12.7 11.9 0.59

Score Large lesion Small lesion

FNC sampling Mair score 5.57 3.5 0.06

FNC sampling modified Mair score 12.7 9.28 0.03*

FNA Mair score 5.17 2.83 0.02*

FNA modified Mair score 11.9 8.5 0.02*

Benign disease Malignant disease

Mean FNC sampling Mair score 3.50 4.27 0.39

Mean FNA Mair score 2.61 3.79 0.15

Mean FNC sampling modified Mair score 10.7 12.4 0.32

Mean FNA modified Mair score 9.28 11.8 0.10

*p < 0.05.

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Discussion

Standard FNA technique in EUS-guided biopsy usesthe application of a 10-mL syringe-derived pressure todraw cells into the needle lumen. The negative pres-sure is thought to stabilize the target tissue firmlyagainst the cutting edge of the needle and increasesthe quantity of specimen obtained.2 It has been sug-gested that FNA with a suction force > 10 mL mightfurther increase cellular yield; however, the data thusfar has been disappointing. In one study, FNA oflymph nodes using different quantities of suction (10,20 and 30 mL) demonstrated that standard suctionwith 10 mL provided maximal specimen cellularity.15

Another study examined the use of 35 mL of suctionapplied in a heterogeneous group of lesions (17 pan-creatic, 5 mediastinal and 5 miscellaneous) generatedby an Alliance II inflation system (Microvasive En-doscopy, Boston Scientific Corp., Natick, Massachu-setts).16 No difference in accuracy was seen betweensamples obtained with high suction or standard FNA.Specimen quality was not evaluated.

FNC sampling is a biopsy technique that does notuse an external suction force. Although some largecenters use FNC sampling as their primary biopsymethod,4 no clear advantage of it over FNA in EUS-guided biopsy has been demonstrated in clinical stud-ies. Before the advent of EUS, FNC sampling wasevaluated in percutaneous biopsy of the breast. A com-bined experience of over 8,500 patients demonstratedthat adequate cellular material could be obtained in> 94% of lesions6 with accuracy as high as 99.6% whenan onsite cytopathologist was present.14 A direct com-parison of FNC sampling and FNA performed in 100consecutive superficial masses showed the quality ofFNC samples to be superior to that of FNA.5 Al-though FNA was found to have a higher accuracy thanFNC sampling, this was not statistically significant.Some studies have suggested that FNC may be betterin the biopsy of lymph nodes,7,8 whereas FNA mayyield better specimens in pancreatic masses and scle-rotic lesions.9 However, these data are limited.

The only study comparing FNC sampling and FNAin EUS evaluated 43 lymph node biopsies, demon-strating no difference in accuracy between the tech-niques.17 Although cellularity was increased in FNAspecimens, there was no statistical difference. FNAsamples were found to have more blood (p = 0.0004)and lower quality than those obtained with FNC sam-pling. In the study by Wallace et al,17 both techniqueswere not performed on the same lymph node and asimple scale was used to evaluate each node (malig-nancy: +/–; cellularity: 0, 1; quality: serous, serosan-guineous, blood).

In the present study, we directly compared the spec-imen quality of biopsies obtained with FNC sampling

and FNA. We used the score described by Mair et al,5a scale designed specifically to compare samples ob-tained with FNC sampling and FNA (Table I).5 Al-though this scale is the only tool available, criticismsare that the component criteria are highly subjectiveand errors in 1 or more parameters may be signifi-cantly correlated with one another. It has thus beensuggested that a summation of the criteria used in thisstandard score might overestimate diagnostic per-formance. A modified score or adjusted “Kulkarni-Mair” score has thus been recommended to overcomethese limitations.18 We used both the Mair and themodified Mair scores to evaluate our samples, with nostatistical significance between FNC sampling orFNA found in all criteria with either technique (TableIII). Subgroup analysis of pancreatic masses, lymphnodes and malignant or benign lesions also failed toshow any statistical difference. The only differencesobserved were higher Mair and modified Mair scoresin larger lesions compared to smaller lesions in bothFNC sampling and FNA; however, there was no dif-ference observed between techniques in large or smalllesions. This result suggests that specimen quality isnot related to the technique but to size because largerlesions are likely to provide more cellular material,though the data is limited because the sample size ofeach type of lesion is small. FNC sampling providedspecimens with higher mean Mair and modified Mairscores compared to FNA, although this result was notstatistically significant. One interesting finding of ourstudy is that a higher number of passes (> 4) was ableto increase our accuracy from 73.5% to 92.4%. Thisunderscores the importance of obtaining at least 5passes in solid lesions when performing EUS-guidedFNA.

In each lesion, we performed FNC sampling andFNA to allow for a true “head to head” comparison.Our study used FNC sampling as the first biopsymethod in all cases. The design was based on the in-terventional radiology literature, which suggests thatif both methods are to be used, the less traumaticmethod (i.e., FNC sampling) must precede the nega-tive pressure method (FNA) to ensure the initial sam-ples will contain less bloody material and be moreamenable to rapid staining and analysis.2 The draw-back to using this technique is that initial biopsies withFNC sampling may have caused tissue damage andbleeding, putting subsequently collected FNA speci-mens at a disadvantage. The current study thus cannotexclude the possibility that FNA produces a higherquality specimen than FNC sampling. However, be-cause no prior studies have suggested that FNA spec-imens are superior to those obtained by FNC sam-pling, the authors feel that this is unlikely.

The presence of patients with pancreatic masses in

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our study is important because this group of patients isusually the most difficult in which to obtain biopsiesyielding cellular material. One may postulate that suc-tion is important when performing biopsy of a pan-creatic mass because of desmoplastic reaction orchronic pancreatitis within the tumor bed or on thecontrary that suction may deteriorate the quality ofthe slide because of the presence of blood. The au-thors were unable to confirm either hypothesis andsuggest that if a cytopathologist is present for slide re-view, the diagnostic capability of both FNC samplingand FNA can be enhanced.

A limitation of the present study is that the infor-mation was collected retrospectively, but this studydoes contribute quantitatively and qualitatively to thesparse literature for endoscopically reachable solid le-sions. The small sample size limits the study becausesome endpoints may not have been able to attain sta-tistical significance. Not all patients underwent sur-gery, which limits the power of evidence for patientsdetermined to have benign lesions. All lesions studiedwere at least 10 mm in size and most were large (mean29 mm). Suction may be important to help secure theneedle within smaller lesions, which were underrepre-sented in our study. The information collected mayalso have been subject to bias because the endoscopistswere not blinded. The biopsied lesions encompassed abroad range of organ tissues, which may have differentcharacteristics on endoscopic fine needle biopsy.

In conclusion, the present study did not find anydifference in the background blood or clot, amount ofcellular material, degree of cellular degeneration, de-gree of cellular trauma, retention of appropriate archi-tecture, Mair score or modified Mair score betweenFNC sampling and FNA. We recommend that the de-cision to use FNC sampling or FNA in EUS-guidedbiopsy of solid lesions can be left to the discretion ofthe individual endosonographer.

References

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2. Castaneda-Zuniga W (editor): Interventional Radiology. ThirdEdition. Volume 2. Baltimore, Williams & Wilkins, 1997, p1795

3. Das DK: Fine-needle aspiration cytology: Its origin, develop-ment, and present status with special reference to a developingcountry, India. Diagn Cytopathol 2003;28:345–351

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5. Mair S, Dunbar F, Becker PJ, Du Plessis W: Fine needle cytol-ogy: Is aspiration suction necessary? A study of 100 masses invarious sites. Acta Cytol 1989;33:809–813

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10. Haddadi-Nezhad S, Larijani B, Tavangar SM, Nouraei SM:Comparison of fine-needle-nonaspiration with fine-needle-aspiration technique in the cytologic studies of thyroid nodules.Endocr Pathol 2003;14:369–373

11. Kamal MM, Arjune DG, Kulkarni HR: Comparative study offine needle aspiration and fine needle capillary sampling of thy-roid lesions. Acta Cytol 2002;46:30–34

12. Kate MS, Kamal MM, Bobhate SK, Kher AV: Evaluation offine needle capillary sampling in superficial and deep-seated le-sions: An analysis of 670 cases. Acta Cytol 1998;42:679–684

13. Kamal MM, Arjune DG, Kulkarni HR: Comparative study offine needle aspiration and fine needle capillary sampling of thy-roid lesions. Acta Cytol 2002;46:30–34

14. Ceresini G, Corcione L, Morganti S, Milli B, Bertone L, Prampolini R, Petrazzoli S, Saccani M, Ceda GP, Valenti G:Ultrasound-guided fine-needle capillary biopsy of thyroid nod-ules, coupled with on-site cytologic review, improves results.Thyroid 2004;14:385–389

15. Bhutani MS, Suryaprasad S, Moezzi J, Seabrook D: Improvedtechnique for performing endoscopic ultrasound guided fineneedle aspiration of lymph nodes. Endoscopy 1999;31:550–553

16. Larghi A, Noffsinger A, Dye C, Hart J, Waxman I: EUS-guidedfine needle tissue acquisition by using high negative pressuresuction for the evaluation of solid masses: A pilot study. Gastro-intest Endosc 2005;62:768–774

17. Wallace MB, Kennedy T, Durkalski V, Eloubeidi MA, EtamadR, Matsuda K, Lewin D, Van Velse A, Hennesey W, HawesRH, Hoffman BJ: Randomized controlled trial of EUS-guidedfine needle aspiration techniques for the detection of malignantlymphadenopathy. Gastrointest Endosc 2001;54:441–447

18. Kulkarni HR, Kamal MM, Arjune DG: Improvement of theMair scoring system using structural equations modeling forclassifying the diagnostic adequacy of cytology material fromthyroid lesions. Diagn Cytopathol 1999;21:387–393

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