Background Pilot studies indicate that probe-guided resectionof radioactive sentinel nodes (the first nodes that receivedrainage from tumors) can identify regional metastases in patientswith breast cancer. To confirm this finding, we conducted amulticenter study of the method as used by 11 surgeons in avariety of practice settings.
Methods We enrolled 443 patients with breast cancer. The techniqueinvolved the injection of 4 ml of technetium-99m sulfur colloid(1 mCi [37 MBq]) into the breast around the tumor or biopsycavity. "Hot spots" representing underlying sentinel nodes wereidentified with a gamma probe. Sentinel nodes subjacent to hotspots were removed. All patients underwent a complete axillarylymphadenectomy.
Results The overall rate of identification of hot spots was93 percent (in 413 of 443 patients). The pathological statusof the sentinel nodes was compared with that of the remainingaxillary nodes. The accuracy of the sentinel nodes with respectto the positive or negative status of the axillary nodes was97 percent (392 of 405); the specificity of the method was 100percent, the positive predictive value was 100 percent, thenegative predictive value was 96 percent (291 of 304), and thesensitivity was 89 percent (101 of 114). The sentinel nodeswere outside the axilla in 8 percent of cases and outside oflevel 1 nodes in 11 percent of cases. Three percent of positivesentinel nodes were in nonaxillary locations.
Conclusions Biopsy of sentinel nodes can predict the presenceor absence of axillary-node metastases in patients with breastcancer. However, the procedure can be technically challenging,and the success rate varies according to the surgeon and thecharacteristics of the patient.
The histologic status of axillary lymph nodes, one of the mostimportant prognostic indicators in patients with breast cancer,directly affects clinical management.1 However, over 80 percentof women who undergo axillary dissection have at least one postoperativecomplication in the arm, and psychological distress is common.2,3,4,5A potential alternative to axillary lymphadenectomy is sentinel-noderesection.
The first stop along the route of lymphatic drainage from aprimary tumor is a limited set of regional lymph nodes.6 Dyes,radiographic contrast agents, and radioactive tracers have beenused to identify such lymph nodes.7,8,9,10,11,12,13 More than20 years ago, Cabanas proposed that the lymph nodes that firstreceive drainage from a tumor, termed sentinel nodes, couldbe removed by limited surgery and examined to determine whethermore extensive lymphadenectomy should be performed.14 In 1992Morton et al. used a blue dye to identify the lymphatic ductthat drained into the sentinel nodes in patients with melanoma.15Alex and Krag described direct localization of sentinel nodeswith radioactive tracers and a hand-held gamma probe, demonstratingin an animal model that the radioactive-tracer and blue-dyemethods were equally effective in locating lymph nodes.16 Becausethe preliminary results with radioactive tracers were encouragingin patients with melanoma17,18 and patients with breast cancer,19,20we conducted a study in 11 centers to evaluate this method ofidentifying sentinel nodes in patients with breast cancer.
Methods
Patients
Patients were enrolled between May 1995 and September 1997 andgave informed consent. The protocol was approved by an institutionalreview committee at the University of Vermont and at each participatinginstitution. Participating surgeons were trained in the procedurein their own institutions by one of us. Each surgeon performedfive training procedures, the results of which are not partof the analysis. The target for each surgeon was 50 cases.
The inclusion criteria were the presence of invasive breastcancer, clinically negative results from examination of theipsilateral axilla, and a treatment plan that included axillarylymphadenectomy. The exclusion criteria were the presence ofclinically suspicious or overtly abnormal axillary nodes, pregnancy,previous axillary lymphadenectomy, or multiple primary breasttumors.
Radioactive Tracer
Thirty minutes to eight hours before surgery, 1 mCi (37 MBq)of technetium-99m sulfur colloid (CIS-US, Bedford, Mass.) ina volume of 4 ml was injected in divided aliquots at the 3-,6-, 9-, and 12-o'clock positions into the breast tissue surroundingthe primary tumor or biopsy cavity. Technetium-99m sulfur colloidwas prepared according to instructions on the package insert.A hand-held gamma counter (C-Trak, Care Wise Medical Products,Morgan Hill, Calif.) was then used to locate radioactive sentinelnodes. The surgeon first defined the perimeter of the radioactive-tracerdiffusion zone around the injection site, then examined thebreast and surrounding tissue for discrete regions of radioactivity.A "hot spot" was defined as an area of localized radioactivityseparate from the injection site with counts of at least 25per 10 seconds; the measurement was performed before the incisionwas made. Inability to identify a hot spot was considered atechnical failure, even if underlying radioactive sentinel nodeswere subsequently identified.
After all hot spots had been found, an appropriate incisionwas made for an axillary lymphadenectomy. Separate incisionswere made for sentinel nodes outside the axilla. Sentinel nodeswere identified by placing the gamma probe in the wound directlyunder the previously identified hot spot. The surgeon followedthe "line of sight" established by aiming the gamma probe towardthe site of maximal radioactivity emitted from the sentinelnodes and dissecting directly toward the sentinel nodes. Theradioactivity of each excised node was measured with a gammacounter. The radioactive nodes were removed until the backgroundradiation in the bed of the sentinel-node resection site wasless than 10 percent of that of the most radioactive resectedsentinel node.
A conventional lymphadenectomy including level I and II nodeswas then performed: level III nodes were removed if the surgeonconsidered them suspicious. Once removed, the lymphadenectomyspecimen was examined for radioactive nodes. Such nodes werenot considered sentinel nodes. For pathological examination,each sentinel node was processed separately, and the slideswere stained with hematoxylin and eosin. Deep sections and immunohistochemicalstains were not routinely employed.
Statistical Analysis
The rates of technical success for each surgeon and for allpatients are reported with exact 95 percent binomial confidenceintervals. Fisher's exact test for nominal variables and theWilcoxon rank-sum test for ordinal variables were used to comparethe rates of success according to the surgeon, the patient'sage and race, tumor size, location of the primary tumor, typeof tumor, method used to guide the injection, time from injectionto surgery, and type of previous biopsy. A forward variable-selectionmethod was used to examine these same variables in combinationwith 10 indicator variables representing the 11 surgeons todevelop multivariate logistic-regression models to predict technicalfailure. Potential predictors of technical failure were addedto the model if the likelihood-ratio chi-square statistic indicateda significant improvement (P<0.10) in predicting the observeddata. The Hosmer–Lemeshow goodness-of-fit criterion wasused to determine the adequacy of the final model.
For the comparison of the rates of false negative sentinel nodesand true positive sentinel nodes, we used Fisher's exact testand the Wilcoxon rank-sum test, as well as two-sample t-testsfor tumor size and total number of involved nodes. A Spearmanrank-correlation coefficient was used to examine the relationbetween the numbers of pathologically positive sentinel andnonsentinel nodes. Fisher's exact test was used to assess thedistribution of hot-spot locations, given the total number ofhot spots observed for each patient. We used SAS statisticalsoftware21 for data management and statistical analysis, StatXact322 to obtain 95 percent confidence intervals for technicalsuccess rates, and BMDP software23 to develop multivariate logistic-regressionmodels. All reported P values are two-tailed.
Results
Between May 1995 and September 1997, we enrolled 443 women inthe study. The mean (±SD) age of these patients was 56±12years, and 78 percent of them were white. The mean tumor sizewas 1.9±1.3 cm. The tumors were classified in terms ofsubtype as ductal (83.7 percent), lobular (8.6 percent), mixed(2.3 percent), or other (5.4 percent). The surgery performedwas mastectomy (in 31.4 percent of the women) or partial mastectomy(in 68.6 percent).
The mean interval between the injection of the radioactive tracerand surgery was 2.9±1.9 hours. On average, 18.9±6.9lymph nodes were removed from each patient, and the mean numberof sentinel nodes was 2.6±2.2. The overall rate of identificationof hot spots was 93.2 percent, but this value varied significantlyaccording to the surgeon (P=0.001) (Table 1). There was no significantunivariate relation between the successful identification ofa hot spot and the patient's age or race; the size, location,or histologic type of the tumor; the method of injecting thetracer; the interval between injection and surgery; or whetherthe patient had had a prior biopsy.
Table 1. Rate of Technical Success in Identifying a Hot Spot, According to Surgeon, before Incision.
On the basis of statistical modeling, which reflected a goodfit to the data (Hosmer–Lemeshow chi-square=7.5, 8 df;P=0.48), it appears that a prior excisional biopsy, an age of50 years or more, and a primary tumor in a medial location wereassociated with the failure to identify a hot spot (Table 2).These three factors were independent of variables related tothe techniques used by individual surgeons (Table 2).
Table 2. Results of the Logistic-Regression Model Predicting Failure to Identify a Hot Spot.
Among the 413 patients in whom one or more hot spots were identified,the hot spots were limited to one location in 92.7 percent,were in two locations in 6.8 percent, and were in three locationsin 0.5 percent of cases (Table 3). The distribution of hot spotsdiffered, depending on the number of hot spots identified (P=0.001).Overall, the 445 hot spots were found in level I (low axillary)nodes (in 89.0 percent of cases), internal mammary lymph nodes(4.3 percent), level II (midaxillary) nodes (4.0 percent), orother locations. Patients with two or more hot spots tendedto have more internal mammary hot spots and fewer level I hotspots than patients with only one hot spot. A sentinel nodewas not identified underneath the hot spot in 1.9 percent ofpatients (8 of 413).
Table 4 shows the pathological results for the 405 patientsin whom a sentinel node was resected. The observed sensitivityof the finding of a histologically positive sentinel node was88.6 percent (101 of 114); by definition, the specificity was100 percent. The observed accuracy of sentinel nodes for thedetection of metastatic disease was 96.8 percent (392 of 405);the positive predictive value was 100 percent (101 of 101),and the negative predictive value (i.e., the correlation ofnegative sentinel nodes with negative axillary nodes) was 95.7percent (291 of 304).
Table 4. Pathological Status of Sentinel Nodes and Nodes Obtained by Axillary Lymphadenectomy.
The false negative rate did not vary significantly among thesurgeons (Table 5). There were too few false negative results(13) for extensive comparison with true positive results (101)in terms of variables that may have affected the likelihoodof a false negative result. Univariate analysis indicated thatall 13 false negative results occurred when the primary tumorwas in the lateral half of the breast (P=0.004). None of theother variables tested were statistically associated with afalse negative result.
Table 5. Sentinel-Node False Negative Rate According to Surgeon.
There was a significant correlation between the number of pathologicallypositive sentinel nodes and the number of positive nonsentinelnodes obtained at axillary lymphadenectomy (Spearman's rank-correlationcoefficient, 0.49; P<0.001) (Table 6). Among 304 patientswith no positive sentinel nodes, 4.3 percent had nonsentinelnodes that were pathologically positive. Among 95 patients withone to three positive sentinel nodes, 37.9 percent had positivenonsentinel nodes. Among six patients with four or more positivesentinel nodes, 83.3 percent had positive nonsentinel nodes.
Table 6. Relation between Pathologically Positive Sentinel Nodes and Pathologically Positive Nonsentinel Nodes.
Discussion
In this study of a method of identifying sentinel lymph nodesin women with breast cancer by means of a locally injected radioactivecolloid, we found localized radioactivity (hot spots), presumablyrepresenting sentinel nodes, in 93.2 percent of cases. Therewas, however, considerable variation in the rate of successin detecting such nodes among the participating surgeons, evenafter each had performed five training procedures. Before thismethod can be broadly applied in clinical practice, technicalimprovements in identifying sentinel nodes will be necessary.
Injections of the radioactive colloid were more widely spacedaround a prior biopsy cavity than around a primary tumor. Thedeposition of insufficient amounts of colloid between injectionsites may explain why a previous excisional biopsy reduces theprobability of finding a hot spot. Perhaps excisional biopsyshould be avoided if a search for sentinel nodes is planned.
The patient's age and the location of the primary tumor affectedthe success rate of the method we used. In older patients thecapacity of lymph nodes to retain the radioactive colloid maybe decreased, because lymph nodes are replaced by fat in elderlypersons. Increasing the volume of the diluent and the amountof tracer can increase its uptake by sentinel nodes by a factorof 10 and may offset this problem (unpublished data). The relativelyhigh rate of failure to identify sentinel nodes in medial tumorsis probably related to overshadowing (masking) of internal mammarynodes by the injection site.
Among the 405 patients with sentinel nodes, the accuracy ofthe sentinel nodes (the number of cases in which the pathologicalstatus of the sentinel nodes corresponded to the pathologicalstatus of the axillary nodes, divided by the number of cases)was 97 percent. Whereas the positive predictive value was 100percent by definition, the negative predictive value was alsovery good, at 96 percent. These results appear to support, atleast in part, the hypothesis that the status of the sentinelnode can accurately predict whether nodal metastases are present.However, the sensitivity was 89 percent, and the false negativerate for this study was 11 percent.
After injection, the tracer diffuses, resulting in a variablearea of radioactivity with a diameter of several centimeters.Probe counts over this diffusion zone are generally much higherthan those over sentinel nodes. Sentinel nodes located awayfrom the injection site were readily located, because backgroundcounts around the sentinel nodes were low. By contrast, sentinelnodes located near or within the zone of diffusion were notreadily identified, because background counts could exceed thecounts for the sentinel nodes. These two situations highlightthe strengths and pitfalls of probe-guided resection of sentinelnodes: the farther the sentinel nodes are from the tumor, themore readily they are identified, whereas the closer the sentinelnodes are to the tumor, the more difficult they are to identify.
All false negative results occurred when the primary tumor wasin the lateral half of the breast. The control resection wasan axillary lymphadenectomy. To fully test the false negativerate would require a control resection of all possible drainagebasins (internal mammary, infraclavicular, and supraclavicular),which is not feasible. With tumors closer to the potential lymph-nodebasin, technical problems occurred. In the case of a lesionin the lateral half of the breast that drained only to loweraxillary nodes, with at least one cancer-containing sentinelnode that was missed by the probe, a false negative result wouldbe recorded. For this reason, an improved sentinel-node proceduremay not be successful in all patients with breast cancer, evenwith technical modifications. Increasing the volume of tracerinjected can increase the rate of successful identificationof sentinel nodes to 100 percent, according to a report fromone institution.20 Increased volume, which increases the countrate of sentinel nodes (unpublished data), makes the nodes morereadily apparent and should lower the false negative rate whenthe lesion is in the lateral half of the breast. Vital dyesthat provide a visual aid24,25,26 may be complementary to probe-guidedsurgery and lower the false negative rate.
This study may underestimate the number of cases in which primarylymphatic drainage occurs outside the axilla. By using locallyinjected radioactive colloids, Hultborn et al. found a highrate of nonaxillary drainage in patients with breast cancer.27In a study of 250 women without pathologic changes in the breast,there was primary lymphatic drainage to the internal mammarynodes in 20 percent to 86 percent of cases, depending on thequadrant injected.28 Nonaxillary drainage is clinically relevant,because metastases that are exclusive to internal mammary nodesoccur in 5 percent to 10 percent of women with breast cancer.The prognosis is the same for these women as for those withaxillary metastases.29 An autopsy study reported that 90 percentof women who died of breast cancer had metastases in the internalmammary nodes.30 Moreover, a first pleural effusion from breastcancer occurs more frequently on the same side as the breastcancer, suggesting regional thoracic involvement through theinternal mammary nodes.31,32 Probe guidance virtually eliminatesthe morbidity associated with resection of internal mammarynodes and hence may improve the accuracy of node staging byextending the procedure to patients with nonaxillary sentinelnodes.
With probe-guided surgery and the use of colloidal albumin (Nanocoll,Sorin Biomedica, Saluggia, Italy) injected into the parenchyma33or subdermis26 of the breast, the rates of sentinel-node identificationwere 94 percent and 98 percent, and the false negative rateswere 2.3 percent and 4.7 percent, respectively. With blue dyealone injected into the parenchyma of the breast, rates of sentinel-nodeidentification ranged from 65 percent to 93 percent, and falsenegative rates from 0 to 12 percent.25,34
Our reasons for requiring that sentinel nodes be located beforethe incision was made were to document the success rates ofindividual surgeons, allow optimal placement of the incision,and allow accurate targeting in the axillary and nonaxillarynodes. In 3 percent of cases with positive nodes, only nonaxillarysentinel nodes were positive. Removal of nonaxillary nodes hasnot been reported by other investigators. When only blue dyeis used, the incision begins over level I nodes and continuesuntil a blue-stained lymphatic duct is identified. With bluedye, the location of the incision is always the same; however,the location of axillary sentinel lymph nodes varies. To theextent that the location of the nodes varies, so will the amountof dissection. Sentinel nodes that are not in the axilla arenot identified with blue dye.
The completeness of resection of the sentinel nodes was rapidlyconfirmed by placing the gamma detector back into the woundafter removal of the initial sentinel node. When only blue dyewas used, the method of establishing whether multiple sentinelnodes were present was additional random dissection, of whichthe end point is not clear.
On the basis of the results of this study, we conclude thatit is feasible to perform the sentinel-node procedure successfullyin a variety of surgical settings. The procedure can be technicallychallenging, as indicated by the fact that the success ratevaried among surgeons and according to the patients' characteristics.Since the study began in 1995, modifications of the technique,such as increasing the volume of tracer injected, have improvedthe uptake of tracer by the sentinel nodes. Other investigators,using a variety of techniques, have also had good results, andcombining complementary methods may further improve the technicalability to identify all draining sentinel nodes.
Pathological examination of the sentinel nodes revealed thattheir status accurately predicts the status of the axillarynodes. In particular, examination of the sentinel nodes hasgood negative predictive value. However, false negative resultswere observed in the case of lesions located in the lateralhalf of the breast, probably because of the closeness of theinjection site to the underlying sentinel nodes.
By using radioactive tracers, we could identify clinically relevantsentinel nodes outside the axilla; these would have been missedby a conventional axillary lymphadenectomy, since 3 percentof all patients with positive nodes in this series had positivenodes only outside the axilla. On the basis of these results,it is overly simplistic to name a single location as the repositoryof all lymphatic metastases from a primary breast cancer.
Supported by grants (U01 CA65121-02 and P30CA22435) from theNational Cancer Institute.
We are indebted to Ms. Elizabeth Joyce, M.P.A., clinical researchsupervisor; to Ms. Mary Krupski, B.A., research data specialist;and to Mr. Robert Bolyard, records coordinator — all atthe Vermont Cancer Center.
Source Information
From the Cancer Center (D.K.) and the Departments of Surgery (D.K., S.H.), Pathology (D.W.), and Biometry (T.A.), University of Vermont, Burlington; the Sylvester Cancer Center, Miami (F.M.); the Arkansas Cancer Research Center, Little Rock (V.S.K.); Walter Reed Army Medical Center, Washington, D.C. (C.S.); Benedictine Hospital, Kingston, N.Y. (S.F.); Charleston Area Medical Center, Charleston, W.V. (R.K.); Massachusetts General Hospital, Boston (M.G.); Baylor University Medical Center, Dallas (J.K.); and St. Paul Hospital, Dallas (P.B.). Other authors were Pat Whitworth, Jr., M.D., Nashville Surgical Associates, Nashville; Roger Foster, Jr., M.D., Crawford Long Hospital, Emory University, Atlanta; and Kambiz Dowlatshahi, M.D., Rush–Presbyterian–St. Luke's Medical Center, Chicago.The views expressed in this article are solely those of the authors and do not necessarily represent the official views of the National Cancer Institute, the federal government, or the Department of Defense.
Address reprint requests to Dr. Krag at Given Bldg. E309, University of Vermont, Burlington, VT 05405.
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Sentinel-Lymph-Node Biopsy
Schillaci O., Scopinaro F., Abramson L. R., Retsas S., Krag D. N., Moffat F. L., Ashikaga T., McMasters K. M., Edwards M. J., Ross M. I.
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N Engl J Med 1999;
340:317-319, Jan 28, 1999.
Correspondence
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Lambert, L. A., Ayers, G. D., Hwang, R. F., Hunt, K. K., Ross, M. I., Kuerer, H. M., Singletary, S. E., Babiera, G. V., Ames, F. C., Feig, B., Lucci, A., Krishnamurthy, S., Meric-Bernstam, F.
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Balch, G. C., Mithani, S. K., Richards, K. R., Beauchamp, R. D., Kelley, M. C.
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Badgwell, B. D., Povoski, S. P., Abdessalam, S. F., Young, D. C., Farrar, W. B., Walker, M. J., Yee, L. D., Zervos, E. E., Carson, W. E. III, Burak, W. E. Jr
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Koizumi, M., Makita, M., Yoshimoto, M., Kasumi, F., Sakamoto, G., Ogata, E.
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Galimberti, V., Veronesi, P., Arnone, P., De Cicco, C., Renne, G., Intra, M., Zurrida, S., Sacchini, V., Gennari, R., Vento, A., Luini, A., Veronesi, U.
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Swenson, K. K., Nissen, M. J., Ceronsky, C., Swenson, L., Lee, M. W., Tuttle, T. M.
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Meric, F., Buchholz, T. A., Mirza, N. Q., Vlastos, G., Ames, F. C., Ross, M. I., Pollock, R. E., Singletary, S. E., Feig, B. W., Kuerer, H. M., Newman, L. A., Perkins, G. H., Strom, E. A., McNeese, M. D., Hortobagyi, G. N., Hunt, K. K.
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Miller, A. R., Thomason, V. E., Yeh, I-T., Alrahwan, A., Sharkey, F. E., Stauffer, J., Otto, P. M., McKay, C., Kahlenberg, M. S., Phillips, W. T., Cruz, A. B. Jr
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