Original Article
Cytokeratin-Positive Cells in the Bone Marrow and Survival of Patients with Stage I, II, or III Breast Cancer
N Engl J Med 2000; 342:525-533February 24, 2000
- Abstract
Background
Cytokeratins are specific markers of epithelial cancer cells in bone marrow. We assessed the influence of cytokeratin-positive micrometastases in the bone marrow on the prognosis of women with breast cancer.
Methods
We obtained bone marrow aspirates from both upper iliac crests of 552 patients with stage I, II, or III breast cancer who underwent complete resection of the tumor and 191 patients with nonmalignant disease. The specimens were stained with the monoclonal antibody A45-B/B3, which binds to an antigen on cytokeratins. The median follow-up was 38 months (range, 10 to 70). The primary end point was survival.
Results
Cytokeratin-positive cells were detected in the bone marrow specimens of 2 of the 191 control patients with nonmalignant conditions (1 percent) and 199 of the 552 patients with breast cancer (36 percent). The presence of occult metastatic cells in bone marrow was unrelated to the presence or absence of lymph-node metastasis (P=0.13). After four years of follow-up, the presence of micrometastases in bone marrow was associated with the occurrence of clinically overt distant metastasis and death from cancer-related causes (P<0.001), but not with locoregional relapse (P=0.77). Of 199 patients with occult metastatic cells, 49 died of cancer, whereas of 353 patients without such cells, 22 died of cancer-related causes (P<0.001). Among the 301 women without lymph-node metastases, 14 of the 100 with bone marrow micrometastases died of cancer-related causes, as did 2 of the 201 without bone marrow micrometastases (P<0.001). The presence of occult metastatic cells in bone marrow, as compared with their absence, was an independent prognostic indicator of the risk of death from cancer (relative risk, 4.17; 95 percent confidence interval, 2.51 to 6.94; P<0.001), after adjustment for the use of systemic adjuvant chemotherapy.
Conclusions
The presence of occult cytokeratin-positive metastatic cells in bone marrow increases the risk of relapse in patients with stage I, II, or III breast cancer.
Media in This Article
Figure 1
Immunostaining of Occult Metastatic Cells in Bone Marrow with Monoclonal Antibody A45-B/B3 (×1000).Figure 2
Kaplan–Meier Life-Table Analysis of the Survival of Patients with Breast Cancer, According to the Presence or Absence of Micrometastases.Article Activity
- Article
The search for occult metastatic cells in patients with small, curatively resected tumors is of considerable importance, because early dissemination of tumor cells is one of the leading causes of relapse at distant sites1,2 and of death from cancer.3 Immunocytochemical methods to search for occult tumor cells in the bone marrow were originally used in patients with breast cancer,4 but the clinical significance of such cells is controversial. In patients with colorectal,5 gastric,6 and non–small-cell lung7 carcinomas, cytokeratin-specific monoclonal antibodies have been used to identify ectopic epithelial cells in the bone marrow. The presence of these cells was shown to influence the prognosis in patients with these tumors. In breast cancer, antibodies against antigens of the polymorphic epithelial mucin family,8 such as epithelial membrane antigen, human-milk-fat globule, or tumor-associated glycoprotein 12, have been used for this purpose.9-11 However, reports of a positive correlation between clinical outcome and the presence of cells in bone marrow that reacted with these antibodies were questioned when it was found that both epithelial membrane antigen and tumor-associated glycoprotein 12 were expressed not only by epithelial cells but also by plasmacytes and erythroid precursors.12-18 One early study of 49 patients reported that cytokeratin-specific antibodies could detect breast-cancer micrometastases in bone marrow smears.19 These results prompted us to conduct a prospective study using a standardized immunocytochemical technique, a defined number of bone marrow cells, and a monoclonal antibody against an antigen shared by various cytokeratin peptides. Additional justification for the use of cytokeratin-specific antibodies to detect breast-cancer cells in bone marrow is provided by the finding of multiple chromosomal aberrations in cytokeratin-positive micrometastases of cells in interphase by fluorescence in situ hybridization20 or by comparative hybridization of genomic DNA.21 These results demonstrate that cytokeratin-positive cells in the marrow are indeed tumor cells.
Methods
Patients
From January 1994 to December 1997, 743 consecutive patients admitted to the I. Frauenklinik at Ludwig Maximilians University in Munich and the Zentralklinikum in Augsburg, Germany, were studied. Patients underwent bone marrow aspiration from both upper iliac crests after providing written informed consent and before the removal of the primary carcinoma. The procedure was approved by the institutional review boards. The stage and grade of the tumor were classified according to the tumor–node–metastasis classification of the Union Internationale contre le Cancer22 by investigators unaware of the immunocytochemical findings in bone marrow. In addition, immunocytochemical analysis of the bone marrow specimens was performed without knowledge of the histopathological results. In this manner, we examined bone marrow obtained from 552 patients with stage I, II, or III breast cancer; 153 patients with benign lesions of the breast, such as fibroadenomas, mastitis, abscesses, and cysts; 11 with simple cysts; 10 with cystadenoma of the ovaries; and 17 with cervical intraepithelial neoplasms of grade I or II.
In the 552 patients with breast cancer, the primary surgical treatment consisted of breast conservation in 298 and modified radical mastectomy in 254. The tumor was completely resected in all patients, and the routine procedures included dissection of axillary lymph nodes of levels I and II. For the diagnosis of lymph-node metastasis, single embedded lymph nodes were screened at up to three levels. All 298 patients treated with breast-conserving surgery received radiation therapy. Irradiation of the chest wall followed mastectomy in 94 patients. The median absorbed dose in the target area was either 50.0 Gy, given in 25 fractions, or 50.4 Gy, given in 28 fractions (in patients who received concomitant chemotherapy).
Of 170 postmenopausal women with node-positive breast cancer, 72 women who had estrogen-receptor–positive tumors received 20 to 30 mg of tamoxifen daily, and it was recommended that therapy last two to five years. Both premenopausal and postmenopausal patients with estrogen-receptor–negative tumors were treated with chemotherapy. A total of 59 patients with one to three involved axillary lymph nodes received six cycles of chemotherapy consisting of cyclophosphamide (600 mg per square meter of body-surface area), methotrexate (40 mg per square meter), and fluorouracil (600 mg per square meter) every 21 days. In 101 patients who had at least four involved regional lymph nodes, four courses of epirubicin (90 mg per square meter) and cyclophosphamide (600 mg per square meter) were administered, followed by three courses of cyclophosphamide, methotrexate, and fluorouracil. All 19 patients with evidence of inflammatory breast cancer (all of whom had node-positive cancer) received three cycles of chemotherapy before and after surgery, consisting of either epirubicin and cyclophosphamide or epirubicin (90 mg per square meter) and paclitaxel (175 mg per square meter). Of 301 patients with node-negative cancer, 33 received tamoxifen alone, 23 received more than one agent, and 245 did not receive any systemic adjuvant therapy.
At the time of primary surgery, the base-line diagnostic evaluation for distant metastases included plain chest radiography, mammography of the contralateral breast, ultrasonography of the liver, and bone scanning of the entire body. These examinations showed no evidence of distant metastases in any of the patients. After surgery, the patients underwent clinical examinations every three months and were further tested only if they had symptoms. The findings reported here were documented in all patients as of August 16, 1999.
Preparation of Bone Marrow
The procedure for bone marrow preparation has been described previously.16 In short, while the patient was under general anesthesia bone marrow samples were obtained from each upper iliac crest by needle aspiration during primary surgery and stored in heparin-treated tubes. Mononuclear cells were separated by Ficoll–Hypaque density-gradient centrifugation (density, 1.077 g per mole) at 900×g for 30 minutes, the cells were washed and centrifuged at 150×g for 5 minutes, and 1 million cells were placed on each glass slide.16 Aspirates yielded between 4.0×106 and 6.6×107 bone marrow cells (mean, 1.5×107).
Immunocytochemical Analysis
For each patient, we screened 2×106 cells by bright-field microscopy; an identical number of cells served as a control for staining with an irrelevant immunoglobulin. We did not use morphologic features to identify cells; we used only immunocytochemical staining. Because there was no background staining, there were no indeterminate results. All slides were examined independently by two observers who agreed on the results for over 95 percent of specimens. In the case of discrepant results, the two investigators reevaluated the slide and eventually reached a consensus.
We used monoclonal antibody A45-B/B3 (Micromet, Munich, Germany), which is directed against a common epitope on cytokeratin polypeptides, including the cytokeratin heterodimers 8–18 and 8–19,23 at a concentration of 1.0 to 2.0 μg per milliliter to detect tumor cells in cytospin preparations of bone marrow. The specificity of the antibody reaction in the bone marrow specimens was confirmed by the addition of an unrelated mouse myeloma immunoglobulin at an appropriate dilution. The breast-cancer cell line BT-20 served as a positive control for cytokeratin immunostaining.16 The reaction of the primary antibody was developed with the alkaline phosphatase anti–alkaline phosphatase technique combined with the new fuchsin stain24 to indicate antibody binding, as previously described.16
Statistical Analysis
We verified all reported immunocytochemical and histopathological results and reports of events (death, relapse, or recurrent disease) during follow-up by reexamining the original data files. The primary end point was survival, measured from the date of surgery to the time of the last follow-up visit or cancer-related death. Secondary end points were locoregional relapse (including recurrences in the ipsilateral and contralateral breast) and distant metastasis and were measured in the same way as was the primary end point. We constructed Kaplan–Meier life-table curves for survival free of locoregional and distant recurrences and overall survival.25 We used the log-rank test to compare the patients with bone marrow micrometastases with those without micrometastases. Data on patients who were alive and had no evidence of disease at the end of our study were censored. We used Cox proportional-hazards analysis to estimate the prognostic effect of various variables. The variables were entered in a stepwise fashion into the model to compare the independent prognostic value of bone marrow micrometastasis with that of other prognostically relevant variables.26 We used the chi-square test to compare categorical variables. We used the Mann–Whitney U test to assess the differences in the means. A P value of less than 0.05 was considered to indicate a statistically significant difference. All tests were two-tailed. For statistical analyses, we used SPSS software for Macintosh (version 6.1.1).
Results
Detection of Micrometastases
Bone marrow aspirates were obtained from 552 patients with newly diagnosed breast cancer, none of whom had a history of epithelial cancer. Of these patients, 199 (36 percent) had cytokeratin-positive tumor cells in the bone marrow at the time of the initial resection of the primary tumor. In most specimens (185 of 199 [93 percent]) the occult cells were present as dispersed single cells (Figure 1AFigure 1
Immunostaining of Occult Metastatic Cells in Bone Marrow with Monoclonal Antibody A45-B/B3 (×1000).); clusters of cells (Figure 1B) were found in only 7 percent of specimens (14 of 199). The overall frequency of occult metastatic cells in each specimen was low; there was a median of 3 cytokeratin-positive cells (range, 1 to 1223) per 2×106 bone marrow cells analyzed. The numbers of detectable tumor cells increased with the tumor stage; for example, patients with stage I cancer had a mean of 5 tumor cells per 2×106 bone marrow cells, and patients with stage II disease and those with stage III disease had means of 9 and 86 tumor cells per 2×106 bone marrow cells, respectively.Bone marrow aspirates from 191 patients with nonmalignant disease were also analyzed in a blinded fashion, before the final histopathological result was disclosed. In only two patients (1 percent) in this group — one with a chronic benign inflammation of the breast and the other with a benign cystadenoma of the ovary — were specifically stained cytokeratin-positive cells detected.
Characteristics of the Patients
Table 1Table 1
Clinical Characteristics of 552 Patients with Breast Cancer, According to the Presence or Absence of Occult Metastatic Cells in Bone Marrow. shows the clinical characteristics of the study population. Most patients (58 percent) had primary tumors that were no more than 2 cm in diameter. Larger primary tumors were associated with a higher incidence of micrometastases than were tumors that were 2 cm or less in diameter (P<0.001). Of 43 patients with stage pT4 tumors (invasion of contiguous structures), 19 had inflammatory breast cancer; 15 of these 19 patients (79 percent) had occult metastatic cells in the marrow (P<0.001). Twenty-three percent of patients with stage pT1a tumors had occult disease, as did 35 percent of patients with stage pT1b tumors and 30 percent of patients with pT1c tumors (P=0.56 for the difference among the groups).Although histologic involvement of axillary lymph nodes is the standard risk factor used for prognos-tic evaluation, we found that the incidence of bone marrow micrometastases was similar in patients with lymph-node metastasis and those without it (P= 0.13). Of 301 patients without clinical or histopathological signs of lymph-node metastases, 100 (33 percent) had cytokeratin-positive cells in the marrow (Table 1). Table 1 shows that the number of lymph nodes with metastases was significantly associated with the presence of bone marrow micrometastases (P<0.001).
Bone Marrow Micrometastases and Recurrence of Disease
After a median follow-up of 38 months (range, 10 to 70), relapse of the tumor occurred in 135 patients: 28 of these women (21 percent) had locoregional relapse, and 107 (79 percent) had distant metastases. Whereas locoregional relapses were not associated with the presence of micrometastases in bone marrow, as compared with their absence (relative risk of relapse, 0.89; 95 percent confidence interval, 0.39 to 2.01; P=0.77), distant metastasis was significantly associated with the presence of occult micrometastases in the marrow (Figure 2AFigure 2
Kaplan–Meier Life-Table Analysis of the Survival of Patients with Breast Cancer, According to the Presence or Absence of Micrometastases.). Of 33 patients with relapses at visceral sites, 13 had bone marrow involvement. In contrast, micrometastases were found in 18 of 19 patients with relapses in the skeleton and in 48 of 55 patients with relapses at visceral sites in combination with skeletal metastases (P<0.001).Bone Marrow Micrometastases and Survival
Of 199 patients with occult metastatic cells, 49 died of cancer-related causes (25 percent), whereas of 353 patients without occult tumor cells in the marrow only 22 died of breast cancer (6 percent). As shown in Figure 2B, patients with bone marrow micrometastasis had a higher risk of death from cancer than patients without bone marrow micrometastases (relative risk, 4.28; 95 percent confidence interval, 2.59 to 7.09; P<0.001). Among women with cytokeratin-positive cells in the marrow, as compared with those without such cells, the relative risk of death was 3.32 among patients with node-positive cancer (95 percent confidence interval, 1.91 to 5.76; P<0.001) and 13.26 among patients with node-negative cancer (95 percent confidence interval, 3.01 to 58.46; P<0.001) (Figure 2C). Among 100 patients with node-negative cancer and micrometastases, 14 (14 percent) died of cancer-related causes, whereas only 2 patients (1 percent) died of cancer-related causes in the group of 201 patients without micrometastases. There was no significant difference in survival, however, between patients with node-negative cancer who had micrometastases and patients with node-positive cancer who did not have micrometastases (Figure 2C).
Bone Marrow Micrometastases and Adjuvant Therapy
Since the occurrence of locoregional relapse and distant metastasis may be influenced by adjuvant treatment, we performed a separate analysis of the 245 patients with node-negative cancer who did not receive systemic adjuvant therapy. Of these patients, 81 (33 percent) had occult metastatic cells. Clinically overt distant metastases occurred in 18 of 81 patients (22 percent) with micrometastases (relative risk of distant metastasis, 7.4; 95 percent confidence interval, 2.7 to 19.9; P<0.001), as compared with 4 of 164 patients (2 percent) without micrometastases. Moreover, among the patients who did not receive adjuvant therapy, the relative risk of cancer-related death was higher among the 81 patients with micrometastases than among the 164 without micrometastases (10 deaths [12 percent] vs. 1 death [1 percent]; relative risk, 18.9; 95 percent confidence interval, 2.4 to 70.5; P<0.001).
Among the 51 patients with node-negative cancer who had well-differentiated (grade 1) or moderately well differentiated (grade 2) small tumors (≤1 cm in diameter) that were positive for estrogen receptors, 11 (22 percent) had micrometastases in the marrow. Of these 11 patients, 2 had both locoregional relapse and distant metastases at the time of the last follow-up visit, whereas no such events had occurred among the 40 patients without occult disease. This difference between the 11 patients with micrometastases and the 40 without micrometastases was not statistically significant (P=0.06).
Micrometastases and Other Prognostic Variables
We performed a Cox multiple-regression analysis to determine whether the presence of bone marrow micrometastases was a significant predictor of freedom from distant metastases and of overall survival that was independent of age, menopausal status, tumor size, tumor grade, estrogen-receptor status, and lymph-node status. To control for interactions related to systemic treatment, we stratified data according to the use of adjuvant therapy. No independent factor was identified that predicted locoregional recurrence. In contrast, bone marrow micrometastasis, estrogen receptors, and lymph-node metastasis were each independent predictors of both recurrence with distant metastases and cancer-related death (Table 2Table 2
Results of Univariate and Multivariate Analyses.). On multivariate analysis, the effects of all risk factors decreased markedly, except for the effect of the presence of occult metastatic disease (Table 2).Discussion
In this study of the hematogenous dissemination of breast-cancer cells, we used a monoclonal antibody (A45-B/B3) that binds to an antigen on cytokeratins 8, 18, and 19. These cytokeratins are expressed by normal and transformed epithelial cells23,27 but not bone marrow cells.16,17 As compared with antibod-ies against single members of the cytokeratin family, A45-B/B3 is more sensitive,16,17 perhaps in part because of the down-regulation of individual cytokeratin polypeptides in some transformed cells.28 The finding of multiple tumor-specific chromosomal aberrations in cytokeratin-positive cells in bone marrow is strong evidence that our method detects micrometastases.21,29
The controversy over the prognostic relevance of the presence or absence of cytokeratin-positive cells in the marrow9-11,19,30-33 may be explained by the use of different antibodies, staining techniques, and criteria for defining positively stained cells. The absence of detectable cytokeratin-positive cells in 189 of 191 specimens from control patients with nonmalignant disease in our study (with all analyses performed in a blinded fashion) demonstrates the specificity of A45-B/B3. The two positive results may have been caused by staining of plasmacytoid cells,34 or they may reflect the presence of an occult malignant tumor.14 The specificity of cytokeratin as a marker of epithelial cancer cells seems clear,35 but there remains the problem of the sampling error inherent in examinations of small volumes of aspirated bone marrow. The exclusion of samples with less than the median number of tumor cells (e.g., 3 tumor cells per 2×106 marrow cells) from our analysis did not change the statistical significance of our findings. Moreover, in vitro experiments showed that our assay reproducibly detected a single tumor cell among 1 million bone marrow cells (unpublished data). In this study, we examined a median of 2 million marrow cells from each patient.
The shortcomings of current tumor-staging practices are revealed by the facts that distant metasta-ses eventually occur in up to 30 percent of patients with node-negative cancer36 and that approximately 40 percent of patients with node-positive cancer survive for 10 years or more.37,38 Ménard et al. reported that the presence of lymph-node metastases was not a reliable prognostic indicator in biologically defined subgroups of patients,39 suggesting that lymph-node metastases are not necessarily associated with hematogenous spread of cancer. After four years of follow-up, we found that the presence of occult micrometastases in the marrow was associated with a statistically significant reduction in overall survival. Among patients without such micrometastases, overall survival at four years was 93 percent, whereas among patients with one or more cytokeratin-positive micrometastatic cells, it was 68 percent. This association with overall survival was observed in patients with lymph-node metastases and in those without them, as well as in patients who did not receive adjuvant chemotherapy. The effect of the presence of occult micrometastases was especially clear among patients with node-negative cancer, whose overall survival was similar to that of patients with node-positive cancer who did not have micrometastases. Moreover, the presence of cytokeratin-positive cells in bone marrow was associated with a significantly higher risk of distant metastases but not of locoregional recurrences. In particular, skeletal relapse was strongly related to the presence of micrometastases, suggesting that precursor cells of overt metastases may indeed be present among the dispersed cytokeratin-positive cells we detected in the marrow at the time of diagnosis.
Whether patients with bone marrow micrometastases respond differently to adjuvant chemotherapy than patients without micrometastases remains to be studied. However, we have previously demonstrated that the proliferation rate of micrometastases (which might influence their sensitivity to chemotherapy) appears to be rather low.40 In addition, micrometastases in bone marrow are frequently found after chemotherapy, and their presence increases the risk of relapse.41 Because 245 of the 301 patients with node-negative cancer in our study did not receive systemic adjuvant therapy, the influence of occult metastatic cells on prognosis could be assessed independently of such therapy. We believe that the risk of relapse among patients with node-negative cancer who have bone marrow micrometastases may be sufficiently high to warrant the administration of adjuvant chemotherapy.
Our findings support the view of Fisher and colleagues,42 who maintained that different pathways of tumor-cell dissemination cause distinct patterns of metastasis. In line with this reasoning are the results of immunohistochemical studies of lymph nodes of patients presumed to have node-negative breast cancer43,44; these studies found no concordance between the presence of lymph-node metastasis and the presence of bone marrow micrometastases. Analysis of the different metastatic routes that independently predict clinical relapse may provide complementary prognostic information.
Two recent studies have shown that the long latency period between diagnosis and relapse in patients with breast cancer, even in those with node-positive cancer, may signal the need to monitor these patients for 10 to 15 years to assess the influence of occult metastatic cells on survival.37,38 For this reason, we caution against the overinterpretation of our data, especially in the case of patients with node-negative cancer who have occult metastatic cells, since we have only four years of follow-up data available. Nevertheless, the finding of such cells far from the primary tumor should alert the physician to the possibility of a subsequent relapse. Whether cytokeratin-positive cells in the marrow are really precursors of metastasis may be answered in the future by genomic studies of single cells or by analyses involving gene profiling.21 With respect to therapeutic strategies whose aim is to prevent metastatic disease, the detection of bone marrow micrometastases may become a useful means of stratifying risk in the heterogeneous group of patients with node-negative breast cancer.
Supported by the Dr. Mildred Scheel Foundation, Bonn; Wilhelm Sander Stiftung, Munich; the Freunde der Maistrasse Foundation, Munich; the Curt Bohnewand Foundation, Munich; and the Friedrich Baur Foundation, Munich.
We are indebted to Beate Zill (Munich) and Susanne Ehnle (Augsburg) for their excellent technical assistance and to all our colleagues at the departments of gynecology and obstetrics in Munich and Augsburg and the department of general surgery in Augsburg (head, Professor Jens Witte) for their help in recruiting and following the patients.
Source Information
From I. Frauenklinik, Klinikum Innenstadt (S.B., W.J., F.H., C.R.M.K., S.G., T.D., G.K.), and the Institut für Immunologie (G.R.), Ludwig Maximilians University, Munich; Frauenklinik, Universitätsklinikum Eppendorf, Hamburg (K.P.); and II. Medizinische Klinik (P.M., G.S.) and Frauenklinik (A.W.), Zentralklinikum Augsburg, Augsburg — all in Germany.
Address reprint requests to Dr. Braun at I. Frauenklinik, Klinikum Innenstadt, Ludwig Maximilians University, Maistrasse 11, D-80337 Munich, Germany, or at sbraun@fk-i.med.uni-muenchen.de.
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