Original Investigations

Mammographic Appearance of Breast Cancer in

African-American Women: Report of 100 Consecut ive Cases 1

Stephanie K. Patterson, MD, Mark A. Helvie, MD, Lynn K. Joynt, MD Marilyn A. Roubidoux, MD, Myla Strawderman, MS

Rationale and Objectives/The authors determined the mammographic appearance of breast carcinoma in Afri- Can-Amaerican women and compared it with that in a white Cohort. i

Materials and Methods. The authors reviewed the mammograms, clinical records, and pathology records of 97 consecutive African-American women with 100 con- firmed breast cancers and 110 white women with 111 confirmed breast cancers.

Results. The mammograms Obtained in African-Ameri- canwomen were positive in 94 cases (94%), and those obtained in white women were positive in 99 cases (89%). Forty-seven percetat of malignancies in African- American women appeared as calcifications, aloneor with a mass, and 41% appeared as a mass only. There Was no statistically significant difference in the Ire= quency of these two findings betweent_he African- American and the white populations. There was no statis- tically significant difference in the breast parenchymal pattern between the two groups. The most common tu- mor location in both races was the upper outer quadrant2

C0uelusion. Breast carcinoma in African-American women is similar to that in white women in terms of

• mam_mographi c appearance, location, and breast density. 'i The matmmograpbic appearance should notbe an impedi- ment to the detection of breast cancer in African-Ameri- can women.

Key Words, Breast neoplasr~s, diagnosis; breast radiog- raphy. ~

Acad Radio11998; 5:2-8

1 From the Departments of Radiology/TC2910 (S,K,P., M.A,H., L.K.J., M.A.R.) and Biostatistics (M,S.), University of Michigan Hospitals, Com- prehensive Cancer Center, 1500 E Medical Center Dr, Ann Arbor, MI 48109-0326. Received April 30, 1996; revision requested June 14; revi- sion received September 18, 1997; accepted September 26. Address reprint requests to S, K.P,

©AUR, 1998

Although the incidence of breast cancer is increasing in both the white and African-American populations, the

mortality rates are higher in African-American women

than in white women (1-6). Whereas breast cancer mor-

tality rates declined 4.7% for American women as a whole between 1989 and 1992, the mortality rate for Af-

rican-American women increased 2.6% in the same pe-

riod (7). Socioeconomic status, stage of disease at diag-

nosis, diagnostic and treatment delays, treatment differ-

ences, and biologic characteristics of breast cancer have

been explored as possible causes of this disparity (1-6).

African-Americans account for 13% of the U.S.-popula-

tion (8). To our knowledge, the utility of mammography in Af-

rican-American women has never been studied in a ran-

domized trial and the mammographic appearance of

breast cancer in these women has not been described. In a recent population-based study, screening mammography

was not beneficial in African-American women for the

protection against advanced disease stage (9). The pur-

pose of our study was to determine the mammographic

appearance of breast cancer in African-American women

and compare it with that in a white cohort.

A search of the computerized database of our multidisciplinary Breast Care Center resulted in finding

143 women who identified themselves as African-Ameri-

can or black and in whom biopsy-proved breast cancer was

diagnosed between June 1986 and March 1995. Patients

with lobular carcinoma in situ were not included. During

the same period and from the same database, 186 of 2,059

women who identified themselves as Caucasian (white) were randomly selected for comparison after matching for

year of diagnosis by using a random numbers table.

Table 1 Appearance of Breast Cancer according to Mammographic

Race

Mammographic African-American Appearance Women White Women

Calcifications alone 18 (18) 26 (24) irregular mass 24 (24) 18 (16) Spiculated mass 10 (10) 20 (18)

Circumscribed mass 7 (7) 7 (6)

Asymmetric density 4 (4) 6 (5)

Architectural distortion 2 (2) 3 (3)

Calcifications present with another feature

Total 29 (29) 18 (16) With circumscribed mass 1 (1) 1 (1) With irregular mass 11 (11) 1 (1) With spiculated mass 9 (9) 9 (8) With architectural distortion 3 (3) 4 (4) With asymmetry 5 (5) 3 (3)

Negative 6 (6) 12 (11) Total 100 110

i i

Note. - -bata expressed as number of tumors. Numbers in parentheses are percentages.

Of the 143 African-American women, 105 had mam- mograms or mammogram reports available for review.

Eight women were excluded because they had recurrent cancers or their files lacked sufficient clinical informa- tion for review. Thus, there were 97 African-American

women with 100 malignancies in this study. Seventy-six of the 186 white women were excluded

owing to unavailability of mammograms or mammogram reports or because of insufficient clinical data; thus, there were 110 white women with 111 malignancies in our

study. Sixty of the 97 African-American women (62%) and

48 of the 110 white women (44%) were initially referred

from an outside institution. African-American patients were between 27 and 82 years old (median, 53 years;

mean, 55 years), and white patients were between 29 and 86 years old (median, 59 years, mean, 58 years).

Mammography at our institution was performed by us-

ing a conventional screen-film technique with dedicated

equipment (model CGR DMR, 600 T500 T, GE Medical

Systems, Milwaukee, Wis; or DC MAG, Mammex, Bayshore, NY) with standard screens (Min-R; Eastman

Kodak, Rochester, NY), single-emulsion film, and dedi-

cated processing equipment. The mammograms of the re- ferred patients were obtained with unknown but dedicated

mammographic equipment. In some of these patients, supplemental mammograms were obtained at our institu-

tion as part of their referral evaluation. Mammograms were retrospectively reviewed for the

presence of radiographic signs of malignancy by two ra-

diologists with fellowship training in mammography. In some cases, the mammograms were not available for ret-

rospective review but had been previously reviewed at the time of examination, where the mammographers at our institution had generated a report; in these cases, the mammographic report was reviewed. Tumor size was de- termined on the basis of the maximum mammographic dimension of invasive tumors. The mammographic ap-

pearance of the malignancies was evaluated and assigned

to one or more of seven categories, as follows: calcifica- tions, circumscribed mass, irregular mass, spiculated mass, architectural distortion, asymmetry, or negative. These categories are based on the Breast Imaging Report-

ing and Data System of the American College of Radiol- ogy (10). The distinction between the different masses was based on the prevalent pattern involving at least 75% of the borders. The breast and quadrant location of each malignancy were documented. Tumors were classified as multifocal if lesions in the same breast occurred at least 2 cm apart on the mammogram (11). The breast parenchy-

mal pattern was evaluated and categorized into one of four patterns, as follows: predominantly fatty, scattered

fibroglandular densities, heterogeneously dense, and ex- tremely dense.

Screened patients were defined as women in whom a negative mammogram had been obtained within the pre-

vious year (_+6 months). Nonscreened patients were de- fined as women who had not undergone mammography

within the past 18 months (two African-American women, aged 40 and 49 years, who had a negative mam- mogram 19-24 months prior to diagnosis were considered nonscreened; in three white women in this same age group, negative mammograms had been obtained 19-24 months prior to diagnosis, and these women were consid-

ered nonscreened). Twenty-two African-American women were classified as screened (13 at our institution), and 75 were classified as nonscreened. Thirty-two white women were classified as screened (20 at our institution),

and 76 were classified as nonscreened. In two white women, the screening status was unknown. The differ- ence in the proportion of screened women between the two groups was not statistically significant (P = .271). All

patients who underwent screening mammography at our

institution also underwent physical examination of the

breast. Palpable lesions were documented as present if

noted at physical examination by the patient, physician,

or mammography staff. A pathologist at our institution reviewed histologic slides of all outside cases. Histologic

results and axillary lymph node status were recorded. The patients' menstrual status--including whether they were

premenopausal, postmenopausal receiving estrogen re-

placement, or postmenopausal without estrogen replace-

men t - -was also recorded. The proportions of African-American and white pa-

tients with certain characteristics on their mammograms

were compared with the Fisher exact test by using Stat-

Xact software (Cytel Software, Cambridge Mass). The

size of invasive tumors was compared with the Wilcoxon

rank sum test (SAS procedure NPAR1WAY; SAS Insti-

tute, Cary NC). All P values are two-sided.

Mammograms obtained in African-American women

were positive in 94 of the 100 cases (94%), and those ob-

tained in white women were positive in 99 of the 111 cases

(89%). The mammographic appearance of the cancers in

both groups is described in Table 1, and the mammo-

graphic appearance in screened and nonscreened patients is

described in Tables 2 and 3, respectively, and all the data

in the Tables is based on number of malignancies, not number of women. The file of one white woman was miss-

ing information about the mammographic appearance of

her tumor, and she was excluded from this analysis. There

was no statistically significant difference between the two

racial groups overall with regard to malignancies with cal-

cifications, either alone or together with a mass (P = .331), or malignancies that appeared as a dominant mass only (P

> .999) (Table 1). The difference between the proportion of African-American and the proportion of white women

with calcifications and another feature was statistically sig-

nificant (29% vs 16%, P = .031). This finding is probably

due to the fact that a greater proportion of African-Ameri-

can women had tumors described as calcification with an irregular mass (11% vs 1%). In fact, the proportion of Afri-

can-American women with irregular masses--with or

without calcification--was greater than that in white

women (35% vs 17%, P = .0004). There was no significant

difference between the two groups with regard to the pro-

portion of tumors appearing only as calcifications (P =

.397) or appearing as spiculated (P = .116) or circum-

Table 2 Mammographic Appearance of Malignancies in Screened African-American and White Women

African-American Mammographic Women White Women

Appearance (n = 22) (n = 32)

Calcifications alone 9 (41 ) 5 (16) Irregular mass 5 (23) 7 (22) Spiculated mass 0 (0) 6 (19) Circumscribed mass 1 (5) 1 (3) Asymmetric density 2 (9) 2 (6) Architectural distortion 0 (0) 2 (6) Calcifications present with

another feature Total 3 (14) 7 (22) With circumscribed mass 0 (0) 0 (0) With irregular mass 1 (5) 1 (3) With spiculated mass 2 (9) 3 (9) With architectural distortion 0 (0) 3 (9) With asymmetric density 0 (0) 0 (0)

Negative 2 (9) 2 (6)

Note.--Data expressed as number of patients. Numbers in parentheses are percentages.

scribed (P > .999) masses or in the proportion described as

negative (P = .229).

The proportion of tumors that appeared only as calcifi-

cations was higher in African-American screened women

than in white screened women (41% vs 16%, P = .058)

(Table 2). The proportion of tumors that were spiculated

without calcifications was higher in white women than in African-American women (19% vs 0%, P = .071). How-

ever, no difference was found between the two races with

respect to having a dominant mass (six of 22 African-

American women [27%] vs 14 of 32 white women [44%];

P = .262). Among the nonscreened women (Table 3), Af-

rican-American women had significantly more tumors with calcifications and another feature compared with

white women (33% vs 15%, P = .0008). African-Ameri- can women also had a higher proportion of tumors with

an irregular shape, with or without calcification (37%),

compared with white women (15%) (P = .0002). The

nonscreened African-American women had a smaller pro-

portion of tumors with only calcification compared with nonscreened white women (12% vs 24%, P = .056). The

difference in the proportion of negative mammograms in

this group was marginally significant (P = .096).

The maximum tumor size of the 81 invasive cancers in

African-American women with size information available ranged from 3 to 120 mm (median, 22 mm). The maxi-

mum tumor size of the 78 invasive cancers in the white

Table 3 -. Mammographic Appearar~e 'o fMal ignancies in Nonscreened African-American and White Women

i

African-American Mammographic Women White Women

Appearance (n = 78) (n : 75)

Calcifications alone 9 (12) 18 (24) Irregular mass 19 (24) 11 (15) Spiculated mass 10 (13) 14 (19) Circumscribed mass 6 (8) 6 (8) Asymmetric density 2 (3) 4 (5) Architectural distortion 2 (3) 1 (1) Calcifications present with

another feature Total 26 (33) 11 (15) With circumscribed mass 1 (1) 1 (1) With irregular mass 10 (13) 0 (0) With spiculated mass 7 (9) 6 (8) With architectural distortion 3 (4) 1 (1) With asymmetric density 5 (6) 3 (4)

Negative 4 (5) 10 (13)

Note.--Data are number of patients. ses are percentages.

Numbers in parenthe-

women with size information available ranged from 5 to

80 mm (median, 15 mm). Tumors in African-American

women tended to be larger than those in white women (P

= .007). Of nine tumors larger than 50 mm in the African-

American women, five had diffuse calcifications as the

sole finding or together with an asymmetric density, one

appeared as a diffuse asymmetry due to inflammatory cancer, one was an irregular mass due to squamous cell

carcinoma, one was a diffuse architectural distortion, and

One was a diffuse asymmetry with skin thickening. Of the

six tumors larger than 50 mm in the white women, all but

one had diffuse calcifications alone or together with ar-

chitectural distortion or asymmetric density. In the Afri-

can-American group, 14 of the 100 tumors (14%) were

multifocal and 86 (86%) were not. In the white patients, 10 of the 111 tumors (9%) were multifocal and 101

(91%) were not. Three African-American women had

synchronous, bilateral cancers; two of these women had

multifocal tumors. One white woman had bilateral can-

cers that appeared as diffuse calcifications; it is unclear if there were multifocal tumors.

In the African-American women, 57 of the 100 tumors

(57%) were in the upper outer quadrant of the breast, 14

(14%) were in the lower inner quadrant, 10 (10%) were in

the lower outer quadrant, 15 (15%) were in the upper inner quadrant, and two (2%) were retroareolar. Four patients

had tumors in more than one quadrant. In the white

women, 65 of the 99 tumors (66%) with a known location

were in the upper outer quadrant, six (6%) were in the

lower inner quadrant, eight (8%) were in the lower outer

quadrant, 12 (12%) were in the upper inner quadrant, and

six (6%) were retroareolar. Two white women had tumors in more than one quadrant. Twelve tumors were in an un-

known location in the breast. The most common location in both races was the upper outer quadrant, with more than

50% of the tumors occurring in this quadrant. Overall,

there was no statistically significant difference in the loca-

tion of the tumor between races (P = .209). When we com-

pared upper outer quadrant versus all other locations of the tumor between races, there was still no statistically signifi-

cant association between location and race (P = .148).

The breast parenchymal pattern in seven African-

American women and 10 white women could not be fur-

ther defined. Thus, the pattern in 90 African-American

women was classified as scattered fibroglandular densi-

ties in 23 (26%), heterogeneously dense in 22 (24%), ex-

tremely dense in 21 (23%), and fatty in 24 (27%). In the

100 white patients, the pattern was classified as scattered

fibroglandular densities in 30 (30%), heterogeneously

dense in 34 (34%), extremely dense in 16 (16%), and

fatty in 20 (20%). Overall, there was no statistically sig-

nificant difference in breast parenchymal pattern between

the two groups (P = .265).

Of the 97 African-American women, 57 (59%) were

postmenopausal and were not receiving hormone replace-

ment therapy, four (4%) were postmenopausal and receiv- ing hormone replacement therapy, and 31 (32%) were

premenopausal; in five patients (5%), the hormone status

was unknown. Of the 110 white women, 41 (37%) were

postmenopansal and not receiving hormone replacement

therapy, 26 (24%) were postmenopausal and receiving

hormone replacement therapy, and 31 (28%) were pre- menopausal; in 12 patients (11%), the hormone status

was unknown. Of the premenopausal patients, 12 of 37

African-American women (32%) and 11 of 31 white

women (35%) had extremely dense breasts. Of the

women receiving hormone replacement therapy, none of

the four African-American women and three of the 26

white women (12%) had extremely dense breasts. Of the

postmenopausal patients not receiving hormone replace-

ment therapy, eight of 57 African-American women

(14%) and one of 41 (2%) white women had extremely

dense breasts.

In the African-American women, 34 tumors were nonpalpable and 65 were palpable (one case was indeter-

minate). In the white women, 55 tumors were palpable

5

and 53 were nonpalpable(three cases were unknown).

More women in both race groups with nonpalpable tu-

mors had undergone screening. The median tumor size of

the palpable tumors in the African-American group was 25 mm (range, 8-120 mm). The median tumor size of the

palpable tumors in the white group was 20 mm (range, 5-

80 ram). The palpable tumors in African-American women tended to be larger than the palpable tumors in

white women (P = .053). Tumor sizes were unavailable

for five tumors in the African-American cohort and nine

tumors in the white cohort. Histologic findings are presented in Table 4. Six Afri-

can-American women did not have a more specific histo-

logic finding than adenocarcinoma and were not included

in this analysis. The most common histologic type in both

groups was invasive ductal carcinoma with or without

ductal carcinoma in situ (DCIS). Medullary carcinoma

was significantly more common in the African-American

women than in the white women (9% vs 2%, respective-

ly; P = .046). Of the five African-American women with other tumors, one had a malignant cystosarcoma, one had

a metastatic neuroendocrine tumor, two had squamous

cell carcinoma, and one had both invasive ductal and in- vasive lobular carcinoma in the same breast (the invasive

lobular carcinoma was found in the same specimen). Of

the three white women with other tumors, one had dense

axillary lymph nodes (which were positive for metastatic

breast carcinoma), one had inflammatory carcinoma, and

one had both invasive ductal and invasive lobular carci-

noma in different locations of the same quadrant of the same breast. The difference in the proportion of DCIS

alone between the two groups was not statistically signifi-

cant (P = .3826). Of the 126 women in whom axillary

lymph nodes were sampled for biopsy, 21 of 57 African-

American women (37%) and 24 of 69 white women (35%) had metastatic disease in axillary lymph nodes; the

difference between the two groups was not significant (P

= .853). Thirty-six of 57 African-American women (63%) and 45 of 69 white women (65%) had no axillary lymph

node involvement. The lymph nodes were not sampled for biopsy in 27 of the 97 African-American women

(28%) and 24 of the 110 white women (22%). In 13 of the 97 African-American women (13%) and 17 of the 110

white women (15%), lymph node status was unknown. Of

the women with invasive tumors, 52 of 84 African-

American women (62%) and 64 of 86 white women

(74%) underwent axillary lymph node dissection; four

women from each race group underwent axillary lymph

node dissection for DCIS.

Table 4 Histologic Types of Breast Carcinoma according to Race

African-American Histologic Type Women* White Women

Invasive ducta l carc inoma 32 (34) 42 (38) Invasive ducta l

carc inoma and DCIS 25 (27) 29 (26) DCIS alone 16 (17) 25 (23) Medullary carc inoma 8 (9) 2 (2) Invasive Iobular carc inoma 5 (5) 8 (7) Other invasive carc inoma t 5 (5) 3 (3) Tubular carc inoma 0 (0) 2 (2) Mucinous carc inoma 2 (2) 0 (0) Papillary carc inoma 1 (1) 0 (0)

Total 94 111

Note. - -Data are number of tumors. Numbers in parenthe- ses are percentages. DCIS = ducta l carc inoma in situ.

*Six Afr ican-American women did not have a more specific histologic diagnosis than adenoca rc inoma and are not in- c luded.

tSee text for explanation.

Although the overall incidence of breast cancer is

higher in white women than in African-American women,

the mortality rate with all disease stages is higher for Af-

rican-American women (4,6,12-14). In 1989, the inci-

dence of breast cancer was 109.1 per 100,000 for white

women and 87.8 per 100,000 for African-American

women, yet the mortality rate was 27.5 per 100,000 and 30.4 per t00,000 for white and African-American

women, respectively (6). The greatest difference in the

mortality rate occurs in women younger than 50 years

old, with mortality rates of 5.9 per 100,000 for white

women compared to 9.2 per 100,000 for African-Ameri-

can women (6). Data from the National Cancer Institute

Surveillance and National Center for Health Statistics demonstrated a decrease of 5.5% in the morality rate for

white women but a 2.6% increase in the mortality rate for

African-American women between 1989 and 1992 (7).

Lower socioeconomic status, lack of education about

the importance of screening mammography, lack of phy- sician awareness of screening guidelines, accessibility of

medical services, incomplete acceptance of mammogra-

phy by patients and physician, and biologic, genetic, and

environmental factors are potential reasons for this dis-

crepancy in the death rate between African-American and white women (1,4,12). African-American women seek

treatment for breast cancer in more advanced stages of

6

disease, even when age and~s0cioeconomic levels are controlled for (1,4,13,14). They are also more likely to delay treatment after diagnosis (4,13). Some studies sug-

gest treatment differences as a cause for increased mortal- ity. Other studies, however, have shown little difference

in the natural history of breast cancer between African- American women and white women if appropriate treat- ment is given (4,15).

Other reports indicate several histologic differences. Breast carcinomas in African-American women have less frequent estrogen receptor positivity, poorer differentia- tion, and less fibrosis (16). A recent report suggests dif- ferences in the tumor suppressor gene P-53 (17). An ex- cess of A:T---~G:C transitions in P-53 were found in Afri-

can-American women with breast cancer compared with

white women with breast cancer from the United States and Scotland (17). Regardless of the stage of diagnosis, poorer survival has been found in African-American women compared with white or Hispanic women (18).

Also, African-American women are more likely to have axillary lymph node involvement and a greater number of

positive lymph nodes than white women (18). Lower so- cioeconomic status was not associated with less favorable histologic findings (16). These studies suggest the possi- bility of more aggressive tumor characteristics, which could be acquired or inherited.

Herein, we reported on the mammographic findings of

breast cancer in African-American women and compared them with those in a white cohort. To our knowledge, the mammographic appearance of breast cancer in African- American women has not been described in the radiology literature. The location of breast carcinoma and breast

density were found to be the same in our two groups and

similar to those seen in previous studies based primarily on non-African-American women. Overall, no statisti- cally significant difference was found between our Afri- can-American and white groups, in whom calcification and masses were found in most cases--similar to the findings of other series based primarily on non-African-

American women (11,19). The frequency of calcifications found alone in our screened African-American population

(41%) was higher than that in our screened white group (16%). However, the frequency of calcifications found alone in our African-American population with nonpalp- able malignancies (44%, 15 of 34 patients) is similar to

that reported in studies of nonpalpable malignancies in predominantly non-African-American women (36% and 41%) (11,19). The screened white patients had more spiculated tumors without calcifications than did our

screened African-American patients (19% vs 0%, P =

.071). These differences in our two race groups are likely related to our small sample size of screened women: 22

and 32, respectively. The frequency of a mass found alone in our screened African-American population, how- ever, was not significantly different from that in our

screened white population (27% vs 44%, P = .292). Also, the frequency of a mass found alone in our African- American population with nonpalpable malignancies

(26%, nine of 34 patients) is similar to that reported in a study of predominantly non-African-American women (26%) (11). Because the mammographic appearance of breast carcinoma in our study is similar between our two race groups and to that reported in predominantly non-

African-American women (11,19), this factor does not

appear to impede mammographic detection. Most malignancies were located in the upper outer

quadrant of the breast, with no differences between the two race groups and similar to the 52% reported in a pri-

marily non-African-American population and the 50% reported in the pathology literature (11,20). The distribu-

tion of malignancies among breast parenchymal patterns in African-American women was also similar among our two groups and to that of other non-African-American populations. Sickles (11) described 40% of nonpalpable malignancies in P1 and P2 patterns, 31% in an N1 pat- tern, and 29% in a DY pattern. Therefore, the density of

the breast and the mammographic location of carcinoma do not appear to represent impediments to mammo- graphic detection.

Invasive ductal carcinoma was the most common his- tologic tumor type. However, there was a statistically sig- nificantly greater percentage of medullary carcinoma in

African-American women than in white women (8% vs 2%, P = .046). This finding has been noted in previous reports of poor African-American women (5). This greater percentage of medullary carcinoma may indicate different tumor characteristics.

In a recent study, mammographic screening was not

found to be protective against later-stage diagnosis in Af- rican-American women (as was found in white women)

(9). The lack of a protective effect of mammography in that study was unexpected because underutilization of

screening mammography and physical examination has frequently been proposed to explain the increased diagno-

sis at late-stage disease in African-American women. The lack of a protective effect of mammography persisted when adjusted for multiple factors, including socioeco- nomic status, access to health care, age, obesity, insur-

ance coverage, menstrual history, and family history (9). Differences in the quality of mammography or mammog- raphy reporting were postulated as possible explanations, as were biologic factors. Delay in diagnosis was not ob- served in our study because women were informed of re- sults at mammography, and all were compliant with the recommended surgical management.

In summary, breast cancer in African-American women was found to be similar to that in a white popula- tion and to that reported in previous studies of primarily white populations with regard to mammographic tumor appearance, location, and breast density. Mammographic differences do not explain the reported lack of benefit of mammography to overcome late-stage diagnosis in Afri- can-American women. The efficacy of mammography in this group has not been completely documented.

kCKNOWLEDGMEN"

We thank Shelley McCarthy for data entry and manu- script preparation.

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