intraoperative touch imprint of sentinel lymph nodes in breast carcinoma patients

Intraoperative Touch Imprint of Sentinel Lymph Nodesin Breast Carcinoma Patients

Andrea Lee, M.D.1

Savitri Krishnamurthy, M.D.1

Aysegul Sahin, M.D.1

W. Fraser Symmans, M.D.1

Kelly Hunt, B.S.C., M.D.2

Nour Sneige M.D.1

1 Department of Pathology, University of TexasM.D. Anderson Cancer Center, Houston, Texas.

2 Department of Surgery, University of Texas M.D.Anderson Cancer Center, Houston, Texas.

Address for reprints: Nour Sneige, M.D., Universityof Texas M.D. Anderson Cancer Center, Depart-ment of Pathology, Box 53, 1515 Holcombe Blvd.,Houston, TX 77030; Fax: (713) 794-5664; E-mail:[email protected]

Manuscript received July 26, 2001; revision re-ceived March 11, 2002; accepted March 18, 2002.

BACKGROUND. Sentinel lymph node examination in patients with breast carcinoma

has been gaining in popularity. Currently, there is no standard intraoperative

assessment of sentinel lymph nodes. To assess the utility of an intraoperative touch

imprint (TI) evaluation, the authors compared TI cytology with surface hematox-

ylin and eosin (H&E) histology in sentinel lymph nodes from patients with breast

carcinoma.

METHODS. Sixty five sentinel lymph node biopsy cases were identified. Diagnoses

from TI and surface H&E histologic sections were compared.

RESULTS. Touch imprint had a specificity of 100%, a negative predictive value of

88%, a sensitivity of 65%, and a false negative rate of 9% per sentinel lymph node

biopsy case. Eighty three percent of the false negative TI cases were due to

micrometastasis. Preoperative chemotherapy, primary tumor type, and primary

tumor size did not significantly contribute to false negative events. Touch imprint

identified 67% of the cases that required completion axillary dissection.

CONCLUSIONS. Touch imprint is a reliable and accurate intraoperative technique,

with the potential to save a significant number of patients morbidity and the cost

of a second surgical procedure to remove axillary lymph nodes. The difficulty of

identifying micrometastases appeared to be the major source of false negative

events, a problem that is not unique to TI cytology. Cancer (Cancer Cytopathol)

2002;96:225–31. © 2002 American Cancer Society.

KEYWORDS: touch imprint, intraoperative diagnosis, sentinel lymph node, breastcarcinoma, metastasis.

Lymph node metastasis is the most important prognostic factor inpatients with breast carcinoma. Standard management of patients

with breast carcinoma includes the examination of axillary lymphnodes. Determination of the axillary nodal status usually requiresaxillary dissection and microscopic examination of the lymph nodes.However, axillary lymph node dissection carries a significant risk oflymphedema. Because the status of the sentinel node can accuratelyreflect the status of the remaining axillary nodes,1–3 current treatmentprotocols include the evaluation of the sentinel nodes as an alterna-tive to an axillary dissection. When the sentinel lymph node is nega-tive for metastatic carcinoma, completion dissection of the axillarylymph nodes can be avoided without compromising the patient’stumor staging. As a result, axillary dissection can be limited to thosecases in which the sentinel lymph nodes reveal metastases.

An intraoperative sentinel lymph node assessment would furtherbenefit patients. For example, intraoperative diagnosis of metastasisto the sentinel node would allow the axillary dissection to immedi-ately follow the sentinel node biopsy. This would reduce the risks ofa second surgery, and the patient would have only one recovery

225CANCERCYTOPATHOLOGY

© 2002 American Cancer SocietyPublished online 15 July 2002 in Wiley InterScience (www.interscience.wiley.com).DOI 10.1002/cncr.10721

period. This would also result in elimination of thecost, time, and resources required for a separate pro-cedure.

Intraoperative microscopic assessment of lymphnodes can be accomplished by either frozen section ortouch imprint cytology (TI). Frozen section is the mostcommonly practiced method. However, there are lim-itations to this technique. Frozen sections of fatty lym-phoid tissue can be technically challenging. In addi-tion, freezing introduces immediate and permanentdistortion of tissue histology, which can make thediagnosis of micrometastasis especially difficult onboth frozen and permanent sections.4

Touch imprint, like frozen section, is a quick andreliable technique.4 –12 In most studies, the reportedsensitivity of imprint cytology was comparable to thatof histologic examination by frozen section.6 –14 Al-though there may be advantages to touch imprints,4

its practice is still questionable, and its popularity islimited to a few centers.

Currently, there is no recommended standardmethod for intraoperative sentinel lymph node assess-ment. We undertook the current study to evaluateimprint cytology in the intraoperative setting. Wewanted to examine this technique as a predictor ofmetastasis seen on a single, surface hematoxylin andeosin (H&E) stained section of lymph node.

MATERIALS AND METHODSBetween February 2000 and February 2001, 394 pa-tients with breast carcinoma underwent sentinellymph node biopsy at The University of Texas M. D.Anderson Cancer Center. All sentinel lymph nodesfrom 64 of these patients were intraoperatively evalu-ated by TI cytology; the remaining cases were largelypart of a surgical protocol that required no intraoper-ative evaluation and therefore were not included inthe current study. As soon as the sentinel lymph nodeswere received in the frozen section suite, each lymphnode was serially sectioned into thin, 1—2 mm slicesperpendicular to or along the node’s long axis. Touchimprints were made of each cut surface. The imprintswere either alcohol-fixed (95%) and stained, using thePapanicolaou technique, or air-dried and stained withDiff Quik (Anapath, Lewisville, TX); the choice of slidepreparation method was left to the discretion of thepathologist (SK, AS, WFS, NS). In the current series,the majority of the cases (� 90%) were evaluated byDiff-Quik. All lymph node sections were then fixed informalin and were paraffin-embedded for routine his-tologic evaluation.

The TI cytology was evaluated independentlyfrom the histology sections. A cytotechnologist wasavailable to screen the TI at the request of the pathol-

ogist, if needed. Generally, this was done in cases withmultiple smears to evaluate. The pathologists evaluat-ing the sentinel lymph nodes were within the breastsubspecialty group at M. D. Anderson Cancer Centerand consisted of both surgical pathologists and cyto-pathologists.

Standard histologic evaluation was an H&E sur-face level. Initially, additional H&E levels and/or cyto-keratin immunohistochemistry (cocktail: AE1/AE31:500, Chemicon, Temecula, CA; CAM5.2 1:50, BectonDickinson, San Jose, CA; cytokeratin 1:50, Dako,Carpinteria, CA; keratin 8 and 18 1:30, Zymed, SanFrancisco, CA) could be performed at the discretion ofthe pathologist. These additional studies were usuallyperformed when the surface H&E section had atypicalor suspicious cells. Because the technique of sentinellymph node evaluation is evolving, the current evalu-ation is to perform three deeper H&E sections andcytokeratin immunohistochemistry on the fourth levelon all negative sentinel lymph nodes with negativesurface sections. This protocol was initiated midwaythrough the current study. For the purpose of thecurrent study, the H&E evaluation was limited to thesurface section only.

Because a sentinel lymph node biopsy specimenmay reveal more than a single sentinel lymph node,analysis of the study results was done in relation to thenumber of sentinel lymph nodes obtained (total: 155)as well as the number of cases (total: 65)/axillary nodalstatus. The total number of patients was 64, but onepatient had bilateral sentinel node biopsies. There-fore, the total number of cases was 65. The cytologicand histologic findings of each lymph node and eachcase were categorized as positive for metastatic carci-noma or negative for a tumor. A lymph node wasconsidered positive if the TI or the histology showedmetastatic carcinoma. A case was categorized as pos-itive or negative for metastasis based on the findingsin all sentinel lymph nodes from a single biopsy pro-cedure. Finding any positive lymph node made thecase positive for metastasis.

Cases with atypical or suspicious cells on TI wereintraoperatively considered negative, pending the his-tologic evaluation of permanent sections and possibleimmunohistochemistry. This conservative standardwas used because the patient’s return for additionalsurgery was preferred to an unnecessary axillary dis-section.

The results of TI and histologic findings of surfaceH&E sections were compared, and the false negativerate (false negatives/total number lymph nodes), neg-ative predictive value (true negatives/[true nega-tives � false negatives]), and sensitivity (true posi-tives/[true positives � false –negatives]) of TI were

226 CANCER (CANCER CYTOPATHOLOGY) August 25, 2002 / Volume 96 / Number 4

calculated. The agreement between TI and histologywas tested by a kappa coefficient, which is a measureof agreement with a maximum of 1.00 when agree-ment is perfect and a value of zero when there is noagreement better than chance. The chi-square testwas used to test the independence between TI find-ings and tumor characteristics. The Fisher exact testwas used for the same purpose to test small samples(i.e., when the number of observations expected bychance in each cell of the contingency table was lessthan five). The Wilcoxon rank sum test was used tocompare the continuous variables of tumor size andnuclear grade. Specificity and positive predictive valuewere not discussed, since all positive touch imprintsand histology findings were considered to be true pos-itives (specificity � 100%, positive predictive value �100%).

Representative intraoperative assessments, in-cluding sectioning, imprinting, screening, and the pa-thologist examination, were timed. Approximately30% of the cases were screened by the cytotechnolo-gists.

RESULTSSixty four patients were identified, providing 65 cases.The average age of the patients was 56 years (range,30-85 years). Sixty two patients were female, and twopatients were male. All of the patients had docu-mented invasive carcinoma prior to the lymph nodebiopsy (53 ductal cases, 5 lobular cases, 7mixed cases).The tumor nuclear grades of the primary carcinomaswere as follows: Grade 1, well differentiated (19 cases);Grade 2, moderately differentiated (33 cases); andGrade 3, poorly differentiated (19 cases). The averagesize of the primary tumors was 1.8 cm (range, 0.2-5.6cm). Twenty cases had chemotherapy prior to thesentinel lymph node biopsy (59 sentinel lymphnodes).

One hundred fifty five sentinel lymph nodes wereobtained from these cases. The average number ofsentinel lymph nodes per case was 2.6. Two deeperlevels and a cytokeratin immunohistochemical stainwere obtained in 34 cases (52%), or 82 sentinel lymphnodes (53%). These cases had negative TI and surfaceH&E sections. Although these additional sections wereperformed in some cases, all subsequent mention ofhistology or histologic diagnosis refers to the surfaceH&E section unless otherwise specified.

Thirty two (22%) of 155 lymph nodes were positivefor metastases. Eighteen (12%) were positive by TI,and 31 (20%) were positive by histology. Among the155 lymph nodes, 140 (90%) had the same TI andhistology findings (17 positive, 123 negative). Fourteenlymph nodes were negative by touch imprint but pos-

itive by histology (TI false negative rate, 9%). Onelymph node was negative by histology but positive bytouch imprint (histology false negative rate, � 1%;Tables 1 and 2).

Eighteen (28%) of 65 cases had a positive sentinellymph node biopsy. Twelve cases (18%) were positiveby TI, and 17 cases (26%) were positive by histology.Among the 65 cases, 58 (89%) had the same TI andhistology readings (11 positive, 47 negative). Six caseswere TI negative and histology positive (TI false neg-ative rate, 9%). One case was negative by histology butpositive by TI (histology false negative rate, 2%; Tables

TABLE 3Touch Imprint and Histologic Findings for 65 Cases

Touch imprint

Histology

Negative Positive

Negative 47 6Positive 1 11

Cases refer to axillary nodal status in 64 patients. One patient had bilateral axillary sentinel lymph node

biopsies.

TABLE 4Comparison of Touch Imprint and Histology Findings in 65 Cases

Category No. of Cases (%)

TI � H 58 (89)TI FN 6 (9)H FN 1 (2)

TI: touch imprint; H: histology; FN: false negative.

TABLE 1Touch Imprint and Histologic Findings for 155 Lymph Nodes

Touch imprint

Histology

Negative Positive

Negative 123 14Positive 1 17

TABLE 2Comparison of Touch Imprint and Histology Findings for155 Lymph Nodes

Category No. of nodes (%)

TI � H 140 (90)TI FN 14 (9)H FN 1 (� 1)

TI: touch imprint; H: histology; FN: false negative.

Breast Sentinel Node Touch Imprint/Lee et al. 227

3 and 4). In this case, the only metastasis identifiedwas a single cluster of carcinoma cells on the touchimprint.

There were good agreements between touch im-print and histology (kappa � 0.64 for lymph nodes and0.69 for cases).

The average size of nodal metastases detected was0.4 cm (range, 0.1–1.0 cm). Twenty positive lymphnodes (62%) had metastases � 0.2 cm, and 12 lymphnodes (38%) had micrometastasis (metastasis � 0.2cm; Figs. 1 and 2). Seventy five percent of TI false

negative results were seen in lymph nodes with mi-crometastases (Table 5); TI findings were strongly re-lated with the size of the metastasis (P � 0.01). Thesmaller the metastasis the likelier the false negative TIfindings. Five out of six false negative TI cases weredue to micrometastasis.

Tumor type, size, nuclear grade, and preoperativechemotherapy history showed no influence on TIfindings. The relationship of TI false negatives to tu-mor type and preoperative chemotherapy is shown inTables 6, 7, 8, and 9. The median tumor size was 1.7

FIGURE 1. Micrometastasis seen on

touch imprint (Papanicolaou stain).

FIGURE 2. Micrometastasis seen on

histology (hematoxylin and eosin

section).


cm for the 58 cases in which the TI finding was thesame as the histology finding and 1.4 cm for the 6 TIfalse negative cases (two-sided P value � 0.71). Themedian tumor nuclear grade was 2.0 for the formergroup and 2.0 for the latter group (two-sided P value �0.63).

Positive findings on TI or histology were consid-ered the gold standards for diagnosing metastasis.Therefore, a positive TI or histology finding had a100% specificity and a 100% positive predictive value.The sensitivity of TI for a lymph node was 56%. Thenegative predictive value was 91%. When these pa-rameters were evaluated in relation to cases, the sen-sitivity for TI increased to 65% and the negative pre-dictive value changed to 88% (Table 10). The TIsensitivity for metastasis � 0.2 cm (75% by lymphnode; 92% by case) was better than for micrometasta-sis (25% by lymph node; 58% by case; Table 10).

The average amount of time for a complete intra-operative assessment (imprints, cytotechnologistscreening, and pathologist assessment) varied de-pending on the number of sentinel lymph nodes iden-tified (range, 1-6). However, the evaluations werecompleted within 30 minutes for all the timed cases.This time interval did not result in any delay of patientmanagement. Most patients undergoing sentinellymph node biopsy were also undergoing lumpec-tomy/mastectomy for their primary tumor. The breastresection was performed prior to axillary dissection ifneeded.

DISCUSSIONThe current study shows that TI is a highly reliabletechnique for intraoperative lymph node evaluation,with a 91 % correlation between histology and touchimprint. These findings are similar to those reportedin the literature.4,7,8,12 However, a comparison of thepublished data4,6 – 8,12 (Table 11) shows a wide range offalse negative (� 1–31%) and sensitivity (30-100%)rates, partly due to differences in patient populationsand case selection. For example, in one series,10 theanalysis of data was limited to nodes with no grossevidence of metastasis. Elimination of grossly positivelymph nodes will obviously lower the sensitivity of thetesting method. Similarly, in our practice, breast car-

TABLE 5Relationship of Touch Imprint Findings to Metastasis Size in 32Positive Lymph Nodes

Touch imprint

No. of nodes by metastasis size (%)

> 0.2 cm < 0.2 cm

False negative 5 (25%) 9 (75%)Positive 15 (75%) 3 (25%)

P value � 0.01, Fisher exact two-sided test.

TABLE 6Comparison of Touch Imprint Findings by Tumor Type for 64 Cases

Touch imprint

No. of cases by tumor type (%)

Ductal Lobular Mixed

TI FNa 5 (10) 0 1 (14)TI � Ha 47 (81) 5 (9) 6 (10)

TI FN: touch imprint false negative; TI � H: touch imprint reading the same as histology.a P value � 0.73, Fisher exact two-sided test.

TABLE 7Comparison of Touch Imprint Findings by Tumor Type for 154Lymph Nodes

Touch imprint

No. of lymph nodes by tumor type (%)

Ductal Lobular Mixed

TI FNa 9 (8) 3 (27) 2 (8)TI � Ha 108 (77) 8 (6) 24 (17)

TI FN: touch imprint false negative; TI � H: touch imprint reading the same as histology.a P value � 0.10, Fisher exact two-sided test.

TABLE 8Comparison of Touch Imprint Findings in Relation to PreoperativeChemotherapy for 64 Cases

Touch imprint

No. of cases by preoperativechemotherapy (%)

Yes No

TI FNa 2 (10) 4 (9)TI � Ha 18 40

TI FN: touch imprint false negative; TI � H: touch imprint findings the same as histology.a P value � 0.99, Fisher exact two-sided test.

TABLE 9Comparison of Touch Imprint Findings in Relation to PreoperativeChemotherapy for 154 Lymph Nodes

Touch imprint

No. of nodes by preoperativechemotherapy (%)

Yes No

TI FNa 6 (12) 8 (8)TI � Ha 45 95

TI FN: touch imprint false negative; TI � H: touch imprint findings the same as histology.a P value � 0.55, Fisher exact two-sided test.


cinoma patients are routinely evaluated by ultrasoundas part of their initial staging work up, and any sus-pected nodal metastasis is subjected to fine needleaspiration, thus reducing the number of patients withsizeable nodal metastases who ultimately undergosentinel lymph node biopsy. Therefore, the lower sen-sitivity rate in the current series is probably due tomost of the metastases being small.

In the current series, false negative results signif-icantly correlated with micrometastasis. Similar find-ings have been reported by others.4 – 6,10 A TI samplesonly the cut surfaces of a 2 mm section of tissue. Amicrometastasis is smaller than 2 mm and can occurwithin the tissue section between the two cut surfaces.Thus, false negatives can occur because of samplinglimitations. The identification of micrometastasis is achallenge not only on TI but also on frozen sectionand histology.7,8,10,15 Surface H&E sections are knownto have a false negative rate of micrometastasis. In theseries reported by Ku, the surface H&E sections had afalse negative rate as high as 41%.10 Others haveshown that additional sectioning of the lymph node orspecial studies can increase the identification of mi-crometastasis.16 –18 Midway through the current study,two additional H&E levels and one cytokeratin immu-nohistochemic stain were routinely performed on sen-tinel lymph nodes with a negative surface level. The

additional material on these 82 lymph nodes revealedmicrometastasis in 4 lymph nodes from 4 differentcases that were negative by TI and surface H&E sec-tion (data not shown). The reverse can also happen.Micrometastasis might be identified only on a surfacelevel but will not be present on deeper sections. In thecurrent study, there was one false negative histologyfinding, with the metastasis identified only on the TI.

In the current series, tumor type, grade, and sizeand preoperative chemotherapy did not influence TIresults.

Despite carrying a false negative rate of 9%, ourintraoperative diagnosis of metastasis by TI can beclinically significant. Touch imprint identified 67% ofcases requiring axillary dissection (patients with pos-itive sentinel biopsy). Twelve patients could have hadtheir axillary dissection performed immediately afterthe sentinel node biopsy. The time, monetary costs,and patient recovery period for the additional surgerywould have been eliminated in exchange for intraop-erative assessments on all sentinel node biopsy pa-tients. This could mean significant savings for thepatient and the medical community.

Although the results of TI are similar to thosepublished for frozen section diagnosis of sentinellymph nodes from breast carcinoma patients (sensi-tivity of frozen section ranges from 52-82%),7,9,14 TI

TABLE 10Touch Imprint Statistics in Lymph Nodes vs. Cases

False negative rate Sensitivity Negative predictive value

LN Case LN Case LN Case

Overall 9% 9% 56% 65% 91% 88%Metastasis � 0.2 cm 3% 1% 75% 92% 97% 98%Metastasis � 0.2 cm 6% 8% 25% 58% 94% 92%

LN: lymph node.

TABLE 11Review of Literature on Sentinel Lymph Nodes Touch Imprint in Breast Carcinoma Patientsa

StudyNo. of lymphnodes

False-negativerate (%)

Sensitivity(%)

Specificity(%)

Negative predictivevalue (%)

Current study 155 9 56 100 91Rubio et al., 19985 124 0.8 100 99 96Ku, 199910 381a 9 30 100 88Van Diest et al., 19999 74 31 62 100 74Motomura et al., 20008 153 � 1 96 91 99Cserni, 20014 72 17 83 100 86

a Data were recalculated to match data as presented in the current study. Touch imprints were compared to single hemotoxylin and eosin section except in van Diest et al who used multiple H&E levels and

immunohistochemistry.b Lymph nodes without gross evidence of metastasis.


has advantages over frozen section assessment. Im-prints can be made of all cut surfaces, thus allowingsampling of a larger area, whereas frozen section anal-ysis obtains only a single section from each slice oftissue. Also, the TI technique may be faster becausethere is no freezing or sectioning time. Fatty lymphnodes are no different from cellular lymph nodes toimprint. Most important, the histology of the lymphnode is preserved with TI. Touch imprint does notintroduce artifacts to the tissue; whereas freezing pro-duces significant and permanent distortion artifactswhich may make the diagnosis of micrometastasisespecially difficult during surgery and on final histo-logic sections.

In conclusion, intraoperative TI cytology is a reli-able and accurate technique for the assessment ofmetastatic breast carcinoma in sentinel lymph nodes.Most false negative lymph nodes and cases are due tomicrometastases. Despite the challenge of diagnosingmicrometastasis, TI identifies a significant number ofpatients who require complete axillary dissection.Thus, intraoperative TI may prove to be highly effec-tive for both patients and the medical community.

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intraoperative touch imprint of sentinel lymph nodes in breast carcinoma patients

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