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1 Department of Surgery, Section of General Surgery, Dartmouth-Hitchcock Medical
Center, Dartmouth Medical School and the Norris Cotton Cancer Center, Lebanon,
NH 03756.
2 Department of Community and Family Medicine, Dartmouth-Hitchcock Medical
Center, Dartmouth Medical School and the Norris Cotton Cancer Center, Lebanon,
NH.
3 Department of Radiology, Dartmouth-Hitchcock Medical Center, Dartmouth Medical
School and the Norris Cotton Cancer Center, Lebanon, NH 03756.
Received March 12, 2004;
accepted after revision June 14, 2004.
Supported by the National Cancer Institute (grants CA 23108 and U01 CA
86082-01).
Abstract
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MATERIALS AND METHODS. The study group for this retrospective cohort study consisted of 992 women with invasive breast cancer detected on screening mammography (n = 460) or at physical examination (n = 532) at a single institution between 1990 and 2001. To address the generalizability of study findings, we compared the characteristics of study participants with those diagnosed with breast cancer in a population-based mammography registry.
RESULTS. The patients whose breast cancer was detected on screening
mammography more frequently had lymph nodes free of metastases (84% vs 58%,
p < 0.0001), had smaller tumors (1.5 vs 2.9 cm, p <
0.0001), were more likely to be treated with breast conservation (56% vs 32%,
p < 0.0001), and were less likely to be treated with chemotherapy
(28% vs 56%, p < 0.0001). In a multivariate analysis with
adjustments for age and functional status, patients whose cancer was detected
at physical examination were more than twice as likely to undergo mastectomy
(odds ratio [OR], 2.5; 95% confidence interval [CI], 1.9–3.3) and nearly
three times as likely to be treated with chemotherapy (OR, 2.9; 95% CI,
2.1–3.9). For younger women (40–49 years old), the likelihood of
receiving chemotherapy was more than doubled if the cancer was detected at
physical examination rather than on screening mammograms (OR, 2.3; 95% CI,
1.3–4.0). For older women (
70 years old), patients whose cancer was
detected at physical examination were five times more likely to undergo
mastectomy (OR, 5.8; 95% CI, 3.2–10.5) and four times more likely to
receive chemotherapy (OR, 4.6; 95% CI, 1.6–13) than the group whose
tumors were detected on screening mammography.
CONCLUSION. Breast cancers detected on screening mammography are smaller, are less likely to metastasize to lymph nodes, and are more likely to be treated with breast conservation and without chemotherapy. These findings provide an additional rationale for performing screening mammography, especially for women at age extremes for whom the survival benefit of screening mammography is debated.
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In our study, we sought to evaluate the effect of the mode of breast cancer detection on treatment decisions. Breast cancers detected on screening mammography are smaller and more likely not to have spread to the regional lymph nodes when compared with breast cancers detected at physical examination [7–12]. We hypothesized that patients whose breast cancer is detected on mammography can be treated with less-morbid therapy than patients whose breast cancer is detected at physical examination. The morbidity of treatment includes not only whether patients undergo mastectomy versus breast conservation but also whether patients are treated with chemotherapy.
Adjuvant cytotoxic chemotherapy is recommended commonly to breast cancer patients with lymph node metastases or with tumors greater than 1 cm in diameter, with the exception of the very elderly or those with significant comorbidities [13]. This therapy is associated with several side effects. For example, in one representative cooperative group trial using four cycles of doxorubicin hydrochloride and cyclophosphamide, complications were seen in the following percentages of patients: alopecia, 82%; vomiting, 8%; nausea, 7%; neutropenia, 7%; sepsis, 5%; and severe infection, 4% [14]. More than half of all patients in that study experienced grade 2 or greater toxicity [14]. Furthermore, studies have shown that breast cancer patients undergoing chemotherapy compared with those not treated with chemotherapy are affected by both short- and long-term deficits in memory and learning that are associated with reductions in the quality of life and that persist for as long as 10 years after therapy is completed [15, 16]. Therefore, we undertook a retrospective cohort study to determine whether associations exist between the mode of detection and subsequent treatment.
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To address the generalizability of study findings given that the study
population was ascertained from a single institution, we compared the
characteristics of the women in the study population with the characteristics
of women in a population-based mammography registry that captures information
about more than 90% of women receiving mammography in New Hampshire
[17,
18]. Using similar methods to
those used in identifying women for analysis in the main study, we identified
all cases of invasive breast cancer in the registry for the period of May 1,
1996, to December 31, 2001. We then determined if the cancer was found on
screening mammography or at physical examination. A data file was created that
included the characteristics of the women from the New Hampshire Mammography
Network with the mode of detection as screening mammography or physical
examination, which was identified using an indicator variable. A small
fraction (
10%) of the patients in the New Hampshire Mammography Network
were treated at Dartmouth-Hitchcock Medical Center and therefore also are
included in our study group.
Statistical Analysis
Comparisons between groups (detected on screening mammography vs detected
at physical examination) were made using chi-square and t tests. To
examine the effect of clinical presentation on whether a patient received
mastectomy versus lumpectomy and chemotherapy versus no chemotherapy, we used
logistic regression and adjusted for patient characteristics (age, menopausal
status, and Karnofsky performance status). Analyses were done for the groups
overall and were stratified by age group. We compared data on personal and
tumor characteristics from this study with data from the New Hampshire
Mammography Network using the Mantel-Haenszel test to control for the mode of
presentation. Tests were two-sided, and we considered a p value of
less than 0.05 to be statistically significant.
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Table 2 compares characteristics of the study group, their tumors, and their treatment as a function of the mode of breast cancer detection. Patients whose cancers were detected on screening mammography were slightly older and were more likely to be postmenopausal than patients whose cancer was detected at physical examination. The functional health status of the women in each group was similar, as indicated by their Karnofsky performance status scores. Tumors detected on screening mammography were only half as large as those detected at physical examination (1.5 vs 2.9 cm, p < 0.0001) and were less likely to be node-positive (16% vs 42%, p < 0.0001). Chemotherapy is not recommended for most patients whose tumors are less than 1 cm in diameter and are node-negative [13]. One third of the mammography-detected cancers fell into this category compared with only 7% of the tumors detected at physical examination.
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We observed that patients whose cancers were detected on screening mammography had a lower tumor grade and were less likely to have angiolymphatic invasion (Table 2). In contrast to the marked differences in tumor size and node status, the difference in the percentage of patients whose tumors had increased estrogen receptor was small (85% vs 77%).
Patients whose breast cancer was detected on screening mammography were half as likely to receive chemotherapy as those whose tumors were detected at physical examination (28% vs 56%, p < 0.0001) (Table 2). Furthermore, patients whose cancer was detected on screening mammography were nearly twice as likely to be treated with breast conservation versus mastectomy (56% vs 32%, p < 0.0001). The mode of detection did not affect the likelihood of treatment with tamoxifen.
We also evaluated the subset of 258 patients in the 40- to 49-year-old age group (Table 3). For this group, the tumors detected on mammography were smaller (1.6 vs 2.8 cm, p < 0.0001) and less likely to be node-positive (26% vs 48%, p = 0.001). Whereas only 7% of the 40- to 49-year-old patients with cancer detected at physical examination had tumors that were smaller than 1 cm and node-negative, 33% of those detected on screening mammography fell into this category. The estrogen receptor status of the tumors in each group were similar. As we found with the overall study group, significantly fewer 40- to 49-year-old patients whose breast cancers were detected on mammography were treated with chemotherapy (57% vs 75%, p = 0.003), and more were treated with breast conservation (52% vs 38%, p = 0.03).
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We also evaluated women in the older age group ( 70 years old), and
similar relationships were observed (Table
3). The mean size of the tumors detected on screening mammography
was half as large as that of tumors detected by palpation (1.4 vs 2.9 cm,
p < 0.0001), and these patients were less than half as likely to
be node-positive (12% vs 28%, p = 0.002). Whereas only 7% of the
patients 70 years old or older with cancer detected at physical examination
had tumors that were smaller than 1 cm and node-negative, 39% of those with
cancer detected on screening mammography fell into this group. The estrogen
receptor status of the tumors in the two groups was similar. Significantly
fewer patients 70 years old or older whose tumors were detected on screening
mammography were treated with chemotherapy (4% vs 15%, p = 0.01), and
more were treated with breast conservation (66% vs 27%, p <
0.0001).
Because we found differences in the characteristics of the patients whose tumors were detected on screening mammography versus those whose cancers were detected at physical examination, we performed a multivariate analysis to adjust for patient characteristics so we could determine whether the mode of detection was an independent predictor of treatment. As shown in Table 4, when the data are adjusted for patient age, menopausal status, and functional health status, the mode of detection still had a highly significant effect on the treatment received. After adjustment for patient covariates, women whose tumors were detected at physical examination were nearly three times as likely (odds ratio [OR], 2.9; 95% confidence interval [CI], 2.1–3.9) as women whose tumors were detected on screening mammography to be treated with chemotherapy and were 2.5 times as likely (OR, 2.5; 95% CI, 1.9–3.3) to be treated with mastectomy rather than breast conservation.
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Using this same multivariate analysis to adjust for patient characteristics, we found that women in the 40- to 49-year-old group whose cancer was detected at physical examination were more than twice as likely (OR, 2.3; 95% CI, 1.3–4.0) to be treated with chemotherapy than the group with tumors detected on screening mammography. In multivariate analysis, women in the 40- to 49-year-old age group whose cancer was detected at physical examination were not more likely to be treated with mastectomy (OR, 1.4; 95% CI, 0.8–2.4). In multivariate analysis, women in the 50- to 69-year-old age group whose tumors were detected at physical examination were three times more likely to be treated with chemotherapy (OR, 3.1; 95% CI, 2.1–4.7) and were 2.5 times as likely to undergo mastectomy (OR, 2.5; 95% CI, 1.7–3.8).
The greatest relative differences in treatment were seen in the oldest age group. In multivariate analysis, women in the 70-year-old or older age group whose tumors were detected at physical examination were over four times more likely to be treated with chemotherapy (OR, 4.6; 95% CI, 1.6–13) and more than five times as likely to be treated with mastectomy (OR, 5.8; 95% CI, 3.2–10.5) than women whose tumors were detected on screening mammography.
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Our study found that 36% of women 40–49 years old, 56% of women 50–69 years old, and 49% of women 70 years old or older had their cancer detected on screening mammography. These percentages are higher than those reported in most other studies. Schleicher and Ammon [7] in a 1998 German study found that only 16% of breast cancers were detected on screening mammography. Our increased likelihood of detection using screening mammography may be secondary to the increased use of screening mammography in the general population in our area. In Germany at the time of that study, 30–40% of women underwent screening mammography [7], whereas in New Hampshire approximately 70% of women 50 years old and older have had at least one screening mammogram [18]. The percentage of cancers detected on screening mammography also has been reported to be a function of patient age. For example, in a study that evaluated three regions in the United States, Coates et al. [19] found that only 20% of breast cancers in women 20–44 years old were detected on screening mammography. In contrast, a study of patients 65 years old and older indicated that 76% (99/130) of elderly patients had their tumors detected on mammography [20]. Our study in general supports these findings: A higher proportion of older women had their cancers detected on screening mammography. Our assessment of how the study population relates to a population-based sample of New Hampshire women helps support the generalizability of our findings, because it indicates that no systematic bias based on patient characteristics appears to exist in the data analyzed.
Multiple studies have shown that breast cancers detected on screening mammography are smaller and are more likely to be node-negative than tumors detected at physical examination [7–12]. Our study also found that the mode of detection was associated with dramatic differences in the mean diameters of the tumors and the percentage of patients with positive nodes. Our study has contributed new information in that we found one third of patients with cancer detected on screening mammography had tumors that were smaller than 1 cm in diameter and were node-negative, thereby placing them in a group for whom consensus guidelines would not recommend adjuvant chemotherapy [13]. In contrast, only 7% of patients whose cancer was detected at physical examination fall into this group.
Other studies also have reported that patients whose breast cancer is detected on screening mammography are more likely to undergo breast conservation [7–9, 11, 21]. Rates of breast conservation surgery in the mammography-detected groups in these studies range from 64% to 68%, compared with 45–54% of patients whose tumors were detected at physical examination. Our study confirms this benefit of screening mammography because we found that 56% of patients with cancer detected on screening mammography were treated with breast conservation compared with only 32% in the group with cancer detected at physical examination. We extended these observations by performing a multivariate analysis that adjusted for patient characteristics such as age, menopausal status, and functional health (Karnofsky performance status) and have shown that the mode of detection is an independent predictor of the extent of surgery. After adjusting for patient characteristics that might influence treatment, we found that patients who presented with a palpable mass were still more than twice as likely to undergo mastectomy as patients whose cancer was detected on screening mammography.
To our knowledge, only two previous studies have examined the relationship between the mode of detection of breast cancer and the administration of chemotherapy. Olivotto et al. [9] compared outcomes of women who attended at least one session of the Screening Mammography Program of British Columbia with nonattenders diagnosed with breast cancer. This study did not compare patients whose cancer was detected on screening mammography directly with those whose cancers were detected at physical examination; in fact, only 74% (1,962/2,647) of the cancers in the patients in the screening mammography program were detected on screening mammography, and an unspecified number of patients who did not participate in the screening mammography program had their cancers detected on screening mammography. That study found a statistically significant, but small, difference in the percentage of patients who received chemotherapy: 23% of the screening mammography program participants versus 27% of the nonparticipants.
Haffty et al. [10] evaluated the effect of the method of detection on treatment of patients in the 1980s. The relative difference in chemotherapy rates in their study was similar to ours: Patients were approximately half as likely to receive chemotherapy if their cancer was detected on mammography as those with cancer detected at physical examination. During the time of their study, 11% of the patients with cancer detected on mammography versus 21% of those with cancer detected at physical examination were treated with chemotherapy. Our study confirms and extends these findings. In the time period of our study (1990–2001), adjuvant chemotherapy was being used more frequently: in 28% of the patients with cancer detected on mammography and 56% of those with cancer detected at physical examination. Although the relative difference is the same as that found by Haffty et al., the absolute difference (10% in the Haffty study vs 28% in our study) is much greater, emphasizing the importance of these observations in our current treatment environment. Furthermore, we have extended these observations by using multivariate analysis to show that the mode of detection is an independent predictor of treatment with chemotherapy even when other patient characteristics are taken into account.
Much of the debate concerning the benefits of screening mammography concerns its use in the 40- to 50-year-old age group. Little data are available about the relationship between the mode of detection and therapy for this subgroup of patients. Maibenco et al. [8] showed that, in a group of 40- to 49-year-old breast cancer patients with 119 cases detected at physical examination and 40 on mammography, the mammographically detected tumors were smaller and less commonly node-positive [8]. In their study, patients with cancer detected on screening mammography were more likely to undergo breast conservation (67% vs 50%). Our study, which included 258 patients in that age group, extends their findings. We found that the tumors in the mammographically detected group were significantly smaller and more likely to be node-negative (Table 3). One third of the patients had tumors that were node-negative and smaller than 1 cm in diameter and therefore were not likely to be recommended to undergo chemotherapy. As described by Maibenco et al., we found that patients with cancer detected on screening mammography were more likely to be treated with breast conservation (52%) than patients whose cancers were detected at physical examination (38%). However, this difference was not found to be statistically significant in multivariate analysis when other patient characteristics were taken into account. Nevertheless, our analysis has identified a significant benefit for screening mammography in this patient subset: Patients 40–49 years old whose cancers are detected on screening mammography are less likely to be treated with chemotherapy (57% vs 75%, p = 0.003). This relationship was confirmed by multivariate analysis, which found that patients aged 40–49 whose cancer was detected at physical examination were more than twice as likely to be treated with chemotherapy (OR, 2.3; 95% CI, 1.3–4.0). Our findings provide supportive evidence in favor of screening mammography for women who are 40–49 years old.
Recommendations regarding screening mammography for patients 70 years old and older suffer from a lack of data. Only one study examining the survival benefit of screening mammography, the Swedish Two-County Trial [6], included patients in this age group; women eligible for that study were between 40 and 74 years old. Little data regarding the relationship between the mode of detection and therapy for this subgroup of patients are available. Solin et al. [20] studied a group of breast cancer patients over 65 years old; those researchers found that cancers in 107 patients were detected on screening mammography and cancers in 23 patients were detected at physical examination. Seventy percent of the patients with cancer detected on screening mammography were treated with breast conservation compared with 27% of the patients with cancer detected at physical examination. Our study, which included substantially more patients (113 with tumors detected on mammography; 117, at physical examination), found a similar relationship: 66% of patients with cancer detected on screening mammography were treated with breast conservation compared with only 27% of the patients with cancer detected at physical examination. In multivariate analysis, the mode of detection had the most marked effect on the treatment for elderly patients. Patients 70 years old and older who presented with a palpable breast cancer were over five times more likely to undergo mastectomy and nearly five times more likely to be treated with chemotherapy than elderly patients whose cancer was detected on screening mammography. These findings make a compelling case for the use of screening mammography in elderly patients.
In summary, we have shown in a study of 992 patients that screening
mammography for the detection of invasive breast cancer allows tumors to be
diagnosed at an earlier stage, thereby allowing patients who have developed
breast cancer to be treated adequately with less-toxic therapy. These benefits
are particularly striking in the patients for whom the survival benefits of
screening mammography are most controversial: the 40- to 49-year-old age group
and elderly women ( 70 years old).
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