Original Article
Tumor Angiogenesis and Metastasis — Correlation in Invasive Breast Carcinoma
N Engl J Med 1991; 324:1-8January 3, 1991
- Abstract
- Abstract
Background.
Experimental evidence suggests that the growth of a tumor beyond a certain size requires angiogenesis, which may also permit metastasis. To investigate how tumor angiogenesis correlates with metastases in breast carcinoma, we counted microvessels (capillaries and venules) and graded the density of microvessels within the initial invasive carcinomas of 49 patients (30 with metastases and 19 without).
Methods.
Using light microscopy, we highlighted the vessels by staining their endothelial cells immunocyto-chemically for factor VIII. The microvessels were carefully counted (per 200×field), and their density was graded (1 to 4+), in the most active areas of neovascularization, without knowledge of the outcome in the patient, the presence or absence of metastases, or any other pertinent variable.
Results.
Both microvessel counts and density grades correlated with metastatic disease. The mean (±SD) count and grade in the patients with metastases were 101±49.3 and 2.95±1.00 vessels, respectively. The corresponding values in the patients without metastases were significantly lower — 45±21.1 and 1.38±0.82 (P = 0.003 and P≤0.001, respectively). For each 10-microvessel increase in the count per 200× field, there was a 1.59-fold increase in the risk of metastasis (95 percent confidence interval, 1.19 to 2.12; P = 0.003). The microvessel count and density grade also correlated with distant metastases. For each 10-microvessel increase in the vessel count per 200× field, there was a 1.17-fold increase in the risk of distant metastasis (95 percent confidence interval, 1.02 to 1.34; P = 0.029).
Conclusions.
The number of microvessels per 200× field in the areas of most intensive neovascularization in an invasive breast carcinoma may be an independent predictor of metastatic disease either in axillary lymph nodes or at distant sites (or both). Assessment of tumor angiogenesis may therefore prove valuable in selecting patients with early breast carcinoma for aggressive therapy. (N Engl J Med 1991;324:1–8.)
Media in This Article
Article Activity
- Article
THERE is considerable experimental evidence to indicate that tumor growth is dependent on angiogenesis.1 Thus, after a new tumor has attained a small size of a few millimeters in diameter (about 106 cells), further expansion of the tumor-cell population requires the induction of new capillary blood vessels. These new vessels also increase the opportunity for tumor cells to enter the circulation.2 The induction of angiogenesis is mediated by specific angiogenic molecules released by the tumor and often by macrophages attracted to it.3 , 4 We do not understand how the angiogenic activity is initiated by a given tumor, but it is clear that the switch to the angiogenic phenotype demarcates two stages in the development of a tumor — the prevascular phase and the vascular phase.5 6 7 8 9 The prevascular phase, which has been elucidated in studies of carcinoma of the cervix,7 bladder,8 and breast,9 10 11 12 may persist for years and is usually associated with limited tumor growth (e.g., restricted thickness of melanoma13) and few or no metastases. The vascular phase is usually followed by rapid tumor growth, bleeding, and the potential for metastasis.
The first quantitative evidence that the intensity of angiogenesis in a human tumor could predict the probability of metastasis was reported for cutaneous melanoma.13 14 15 There was a clear distinction between a stage without neovascularization, which correlated with a paucity of metastases, and a stage in which increasing neovascularization correlated with a rising rate of metastasis.
We therefore asked whether the extent of angiogenesis in human breast carcinoma correlated with the occurrence of metastasis. The hypothesis we wished to test was that lesions that have little angiogenesis have a relatively low rate of metastasis, whereas lesions that have entered a higher angiogenic state have an increased probability of metastasis.
Methods
Patients
We studied tumor specimens from 49 patients with primary invasive breast carcinoma. Initially, 26 patients were considered to have positive nodes, and 23 to have negative nodes; subsequently, 4 patients with negative nodes were shown to be positive for distant metastases. The specimens were retrieved from paraffin-embedded tissue of initial breast carcinomas diagnosed at Brigham and Women's Hospital between 1978 and 1983. We selected specimens from approximately equal numbers of patients with positive nodes and patients with negative nodes who had been examined consecutively, who had had invasive breast carcinoma or axillary-lymph-node dissections, and for whom paraffin-embedded tissue blocks and medical records could be retrieved for follow-up studies. Forty-five carcinomas were of an infiltrating ductal type, three were of an infiltrating lobular type, and one was of an invasive tubular type. The patients with distant or lymph-node metastases (n = 30) and the patients without metastases (n = 19) did not differ significantly in tumor grade, tumor size, number of lymph nodes examined, or age (see Statistical Analysis, below). Two tumors were more than 0.5 cm but not more than 1.0 cm in their greatest dimension; 22 tumors were more than 1.0 cm but not more than 2.0 cm; 22 tumors were more than 2.0 cm but not more than 5.0 cm; and 3 tumors were more than 5.0 cm. The tumor size and nodal status were determined from the initial surgical pathology report, and follow-up was obtained by evaluating the patients' charts and by collaboration with the tumor registry of Brigham and Women's Hospital. Tumor sections stained with hematoxylin and eosin were graded according to the Scarff—Bloom—Richardson criteria.16 Five tumors were grade I/III, 22 were grade II/III, and 22 were grade III/III.
Vessel Staining, Grading, and Counting
All blood vessels were highlighted by staining endothelial cells for factor VIII (Dako Polyclonal, Dako, Santa Barbara, Calif.) with use of a standard immunoperoxidase technique described previously.17 Furthermore, areas representative of the invasive component of the cancer were selected from sections stained with hematoxylin and eosin; often, these areas also contained some in situ carcinoma. A section from one paraffin block per tumor was stained for factor VIII.
Microvessel density was assessed without knowledge of the patient's outcome; areas of invasive tumor containing the most capillaries and small venules (i.e., areas of most intense neovascularization) were examined by light microscopy. Tumors were frequently heterogeneous in their microvessel density, but the areas of highest neovascularization were found by scanning the tumor sections at low power (40× and 100×) and identifying the areas of invasive carcinoma with the highest number of discrete microvessels staining for factor VIII (brown). These areas of high neovascularization could occur anywhere in the invasive tumor, but were most frequent at the margins of the carcinoma. Microvessels in sclerotic areas within tumor, where microvessels are sparse, and immediately adjacent areas of unaffected breast tissue were not considered in vessel counts. However, these microvessels served as internal controls in assessing the quality of staining for factor VIII. Only tumors that had high-quality, distinct staining of microvessels (i.e., with low background staining) with use of the immunoperoxidase technique were included in this study. Two tumors were excluded from study because of poor staining.
After the area of highest neovascularization was identified and subjectively graded on a scale of 1 to 4+, individual microvessels were counted on a 200× field (i.e., 20× objective lens and 10× ocular lens; 0.7386 mm2 per field) and a 400× field (i.e., 40× objective lens and 10× ocular lens; 0.1885 mm2 per field). Any brown-staining endothelial cell or endothelial-cell cluster that was clearly separate from adjacent microvessels, tumor cells, and other connective-tissue elements was considered a single, countable microvessel. Vessel lumens, although usually present, were not necessary for a structure to be defined as a microvessel, and red cells were not used to define a vessel lumen. Each count was expressed as the highest number of microvessels identified within any 200× or 400× field. All counts were performed by two investigators using a double-headed light microscope simultaneously; both had to agree on what constituted a single microvessel before any vessel was included in the count. About 5 to 10 minutes was required to assess one tumor. Microvessel counts and density grades were determined without knowledge of the patient's outcome, the presence or absence of metastases, or any other pertinent variable.
Figures 1Figure 1
Area with Highest Density of Microvessels in an Invasive Duct Carcinoma (Panel A) and Representative Benign Breast Stroma Immediately Adjacent to the Carcinoma (Panel B) (Immunoperoxidase Stain for Factor VIII, ×36).A and 2Figure 2
Representative Field of an Invasive Duct Carcinoma That Had Relatively Little Angiogenesis and Did Not Metastasize or Recur (Panel A) and a Representative Area of Benign Breast Stroma Immediately Adjacent to the Invasive Tumor (Panel B) (Immunoperoxidase Stain for Factor VIII, ×36).A show representative fields of invasive carcinomas stained for factor VIII, which contained various numbers of microvessels. For comparison, Figures 1B and 2B show representative fields of adjacent unaffected breast tissue stained with factor VIII. In Figure 1A, the arrows indicate some representative microvessels that were considered distinct and were included in final counts.To assess variability between patients in microvessel counts determined with the technique used in this study, a third investigator repeated the vessel counts (at 200× and 400×) and grading of the same tumors. He was not coached, had no previous knowledge of the counts and grades obtained by the other two investigators, and used only the description and figures provided in this paper. Although the agreement was not exact in every case, linear regression showed that the third investigator's counts correlated highly with those of the other two (density-grading correlation coefficient [r] = 0.61, n = 49, P<0.001; counts at 200×, r = 0.59, n = 49, P<0.001; and counts at 400×, r = 0.62, n = 49, P<0.001).
Statistical Analysis
Because the outcome of interest in our study, metastasis, was either present or absent, we used logistic regression as outlined by Cox.18 We looked for associations between the presence or absence of metastasis and potential prognostic factors, such as microvesseldensity grade, microvessel count, tumor grade, tumor size, and nodal status. This method provides odds ratios or estimates of the relative risk of the presence of metastasis. We first examined univariate relations to determine which factors were related to metastasis, and next performed stepwise multivariate logistic regression to determine whether some combination of variables provided a better estimate of the relative risk of metastasis than any single variable.18
The probability of metastasis was calculated from our logistic-regression model, which basically fit the following equation18:
where P denotes the probability of the outcome (metastasis). However, our model could be simplified: 
where x denotes the vessel count at 200×. With the microvessel count determined at 200×, this model yielded an intercept (constant), a, of -2.614 and a slope, B, of 0.0464. Using these numbers and rearranging the above equation, we calculated the predicted probability of metastasis with a given vessel count according to the following equation: 
For example, if the highest microvessel count per 200× field was 80, the probability of metastasis would be 
Results
Microvascular Density and Metastatic Disease Table 1Table 1
Histologic and Clinical Characteristics of 49 Patients with Breast Carcinoma, According to the Presence or Absence of Metastatic Disease. shows that in the invasive breast carcinomas of the patients with any metastases (to lymph nodes, distant sites, or both), the mean microvessel counts (in areas of highest neovascularization) were 101 per 200× field and 37 per 400× field. In the carcinomas of the patients without metastases, the corresponding values were 45 per 200× field and 17 per 400× field, respectively. Univariate analysis revealed the differences between the groups to be statistically significant (P = 0.003 and 0.004, respectively). Furthermore, with each 10-microvessel increase in the count at 200×, there was a 1.59-fold increase in the risk of metastasis (95 percent confidence interval, 1.19 to 2.12; P = 0.003).The carcinomas of the patients with metastases had a mean microvessel-density grade of 2.95; the carcinomas of the patients without metastases had a grade of 1.38. This difference between the groups was significant (P≤0.001). Furthermore, with each increase in the microvessel-density grade, there was a 5.17-fold increase in the risk of metastasis (95 percent confidence interval, 2.13 to 12.55; P<0.001). Table 1 also shows the values for tumor grade, tumor size, the number of lymph nodes examined, and age. No significant differences were found between the two groups in these four variables.
In the invasive breast carcinomas of the patients with distant metastases only (14 patients), the mean (±SD) microvessel counts were 106±43.6 per 200× field (median, 100.5; range, 38 to 200). In the carcinomas of the patients without distant metastases (35 patients), the corresponding value was 71±48.2 per 200× field (median, 58; range, 15 to 220). The difference between these groups was statistically significant (P = 0.029). For each 10-vessel increase in the microvessel count at 200×, there was a 1.17-fold increase in the risk of distant metastasis (95 percent confidence interval, 1.02 to 1.34; P = 0.029).
The carcinomas of the patients with distant metastases only had a mean microvessel-density grade of 3.0±1.0 (median, 3.0; range, 1 to 4), whereas the carcinomas of patients without distant metastases had a grade of 2.1±1.2 (median, 2.0; range, 1 to 4). This difference was also significant (P = 0.025). With each increase in the density grade, there was a 2.00-fold increase in the risk of distant metastasis (95 percent confidence interval, 1.11 to 3.60; P = 0.025).
The mean microvessel count per 400× field in the patients with distant metastases only was 37±18 (median, 29.5; range, 18 to 74); in those without distant metastases, it was 26±18 (median, 22; range, 6 to 69). The mean tumor grade was 2.4±0.6 in the patients with distant metastases (median, 2.5; range, 1 to 3) and 2.3±0.7 in those without distant metastases (median, 2.0; range, 1 to 3). The mean tumor size was 2.7±1.8 cm in the patients with distant metastases (median, 2.3; range, 0.6 to 8) and 2.5±0.7 cm in those without such metastases (median, 2.0; range, 1 to 9). The mean number of lymph nodes examined was 15.1±11.1 in the patients with distant metastases (median, 13.5; range, 4 to 47) and 13.2±6.4 in those without distant metastases (median, 13; range, 1 to 30). The mean number of positive nodes in the patients with distant metastases was 7.6±12.4 (median, 3.0; range, 0 to 46); in those without distant metastases, it was 1.65±3.7 (median, 0; range, 0 to 20). The mean percentage of positive nodes in the patients with distant metastases was 40.5±40.3 (median, 26; range, 0 to 100); in those without distant metastases, it was 15±27.8 (median, 0; range, 0 to 100). The mean age of the group with distant metastases was 57.7±15.9 years (median, 57.5; range, 25 to 80); in the group without distant metastases, it was 58.8±13.2 (median, 61; range, 38 to 84). No significant differences were found between the two groups in these seven variables. However, a significant difference was noted between the groups in the mean follow-up interval (4.5±3.2 vs. 7.0±3.4 years, P = 0.022; median, 3.5 vs. 8.0; range, 1 to 10 vs. 1 to 11). This finding was not unexpected, since patients without distant metastases lived longer and thus were followed for longer periods.
We next used stepwise multivariate logistic regression to determine whether some combination of variables would provide a better estimate of the relative risk of metastasis than any single variable. By itself, microvessel-density grade provided the best estimate. However, the microvessel-density grade and the microvessel count per 200× field correlated strongly (r = 0.80, P≤0.0001) and provided the same information; thus, they canceled out each other's effect when included in the model simultaneously, instead of interacting to produce a better estimate of the risk.
We plotted the percentage of patients with metastatic disease against the microvessel count divided into progressive 33-vessel increments (Fig. 3Figure 3
Metastatic Disease among 49 Patients in Relation to Microvessel Count in Progressive Increments.). The plot showed that the prevalence of metastatic disease increased as the vessel count increased, reaching 100 percent among patients with invasive carcinomas that had counts of more than 100 per 200× field.Patients with "Negative" Nodes and Distant Metastases
Four patients deserve special emphasis. These patients (17 percent of those with negative nodes) had negative axillary nodes at presentation (T1,N0,M0), but at that time or subsequently had distant metastatic disease and eventually died of breast carcinoma. Three of the four had microvessel-density grades of 3 or 4, but one had a grade of 1; their microvessel counts (per 200× field) were 80, 129, 87, and 140. According to our logistic regression model, these microvessel counts indicated probabilities of metastasis of 0.74, 0.96, 0.79, and 0.97, respectively (see Statistical Analysis).
Angiogenesis around Duct Carcinoma in Situ
Components of duct carcinoma in situ were observed on the slides of 22 patients after immunostaining for factor VIII. A ring of neovascularization around this carcinoma (Fig. 4Figure 4
Area of High-Grade Duct Carcinoma in Situ with (Panel A) and without (Panel B) Periductal Angiogenesis (Immunoperoxidase Stain for Factor VIII, ×18). and 5Figure 5
Large Breast Duct Partially Lined with Duct Carcinoma in Situ and Intense Angiogenesis in Immediately Adjacent Periductal Breast Stroma.) was seen on the slides of five of these patients (23 percent). We interpreted this ring of neovascularization (carcinoma in situ angiogenesis) as representing a response to an angiogenic factor or factors released by the adjacent cells of the duct carcinoma. There appeared to be no relation to periductal inflammation, and in this small sample of patients no clear association with metastatic disease. We present this observation as a case of tumor angiogenesis associated with noninvasive carcinoma.Discussion
These studies showed a significant correlation between the density of microvessels in histologic sections of invasive breast carcinoma stained for factor VIII and the occurrence of metastases. Among the seven patients with a microvessel count of up to 33 per 200× field (i.e., invasive carcinomas with slight neovascularization), one patient (14 percent) had metastases. (The low count for this one patient may reflect a sampling error in paraffin-block selection, since only one block was stained per tumor. Tumors were heterogeneous for density of neovascularization.) In contrast, the occurrence of metastases increased as the microvessel count increased (i.e., a prevalence of 45 percent among tumors with counts between 34 and 67, and 71 percent among those with counts between 68 and 100); 100 percent of patients had metastases when the vessel counts in their tumors exceeded 100 per 200× field.
These results are consistent with the known role of angiogenesis in the metastatic process. For a tumor cell to metastasize, it must breach a series of barriers as well as produce and respond to several growth factors and cytokines.19 20 21 In brief, tumor cells must gain access to the vasculature from the primary tumor, survive travel through the circulation, settle in the microvasculature of the target organ, escape from the vasculature into the target organ, and induce angiogenesis in the target organ. Furthermore, metastases may shed cells to form additional metastases, by following the same cascade of events.21
Angiogenesis is necessary at the beginning of this journey, because without it tumor cells are only rarely shed into the circulation.22 New, proliferating capillaries have fragmented basement membranes and are leaky, making them more penetrable by tumor cells than are mature vessels.23 Furthermore, the invasive chemotactic behavior of endothelial cells at the tips of growing capillaries is facilitated by their secretion of collagenases and plasminogen activator.24 These degradative enzymes may also facilitate the escape of tumor cells into the tumor neovasculature. Finally, to survive and multiply at the site of metastasis, the tumor cells must induce angiogenesis. Angiogenic tumor cells are more likely to arise from a highly angiogenic primary tumor.
Supporting these concepts is an experimental observation made in rabbits. India ink injected into a cornea will stay at the injection site indefinitely as a tattoo, unless neovascularization is induced in the cornea. As new capillaries approach the ink spot, it breaks up and ink particles appear in the ipsilateral lymph nodes.25 These experiments are also consistent with our finding that angiogenesis in breast carcinoma correlates with lymph-node metastasis.
In some ducts containing duct carcinoma in situ, there was also a narrow rim or ring of neovascularization around the duct. We interpreted this ring of neovascularization (carcinoma in situ angiogenesis) as being a response to an angiogenic factor or factors released by the adjacent duct-carcinoma cells. Carcinoma in situ angiogenesis was limited to ducts containing carcinoma in situ and was not associated with periductal inflammation. In fact, Figure 5 shows periductal ring neovascularization immediately adjacent to the portion of the duct containing a focus of the carcinoma in situ; the opposite side of the duct, still lined by normal-appearing epithelium, shows no neovascularization. Since all our biopsy specimens contained elements of invasive cancer, it appears that the angiogenic activity of a tumor can occur independently of invasion. Although some cells of the duct carcinoma in situ became angiogenic, they remained in situ, presumably because they had not yet acquired other properties, such as the ability to breach adjacent basement membranes. If true, this observation underscores the need of a tumor cell to have multiple capabilities to become the agent of a successful metastasis.
We have used the term "onset of angiogenic activity" to describe marked neovascularization present within or at the periphery of a neoplastic focus. This usage should not imply knowledge of a mechanism. Whether capillaries will grow or not grow toward a tumor may depend on one or more events that are not clearly understood at this time. In one model of the switch to the angiogenic phenotype,26 a cancer-suppressor gene that codes for an angiogenesis-inhibitor protein (thrombospondin) is down-regulated when the cells undergo malignant transformation and become angiogenic. Furthermore, Zajchowski et al.27 have shown that somatic hybrid cells produced by fusion of MCF-7 human breast-carcinoma cells with normal immortalized human mammary epithelial cells were suppressed in their ability to form tumors in nude mice. The hybrids had, among other traits like those of their "normal" parent cells, the ability to increase the expression of the angiogenesis inhibitor thrombospondin, supporting the concept that angiogenic capability is important to tumorigenicity in human breast carcinoma. Although several other models are conceivable and much work remains to elucidate the mechanisms by which tumors become angiogenic,4 , 28 , 29 the amount of neovascularization measured directly in histologic sections of breast carcinoma correlates with the presence of metastasis, and this information may prove useful even before we understand why it is true.
Supported in part by a grant (CA-37395–08) from the National Institutes of Health and by a grant to Harvard University from Takeda Chemical Industries. Dr. Weidner is the recipient of a Clinical Oncology Career Development Award from the American Cancer Society.
Source Information
From the Department of Pathology, Brigham and Women's Hospital and Harvard Medical School (N.W., J.P.S., W.R.W.), and the Departments of Surgery and Anatomy and Cellular Biology, Children's Hospital and Harvard Medical School (J.F.), all in Boston. Address reprint requests to Dr. Weidner at the Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, 75 Francis St., Boston, MA 02115.
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