Mammography screening and breast cancer biology in African American women—a review

Cancer Detection and Prevention 26 (2002) 180–191

Review article

Mammography screening and breast cancer biologyin African American women—a review

Renee Royak-Schaler, PhD∗, David P. Rose, MD, PhDDivision of Behavioral Sciences, American Health Foundation, New York, NY 10017, USA

Received 7 January 2002; received in revised form 1 March 2002; accepted 2 May 2002

Abstract

This review examines some of the key issues in early detection and breast cancer biology for African American (AA) women whichcontribute to their diagnoses at more advanced stages than white women, and poorer long-term prognoses. While screening mammographyis considered an essential factor in eliminating these disparities, its optimal application for AAs is not fully understood. There is a paucityof information on the success with which mammography screening programs are maintained over time in the AA population, and onscreening guidelines with regard to age of initiation and frequency. No randomized clinical trials targeting AA women have been reported.This type of information is critical since breast cancer in AA women occurs at younger ages, and frequently demonstrates aggressive tumorbiology at diagnosis. Studies are required to determine the incidence of interval cancers in current screening programs, and the influenceof the biological characteristics which are known to differ in the breast tumors of AA and white women. Recognition of molecular andcellular characteristics which identify the potential invasiveness of ductal carcinomas in situ is also required. These studies would assist inestablishing the criteria for identifying the subpopulation of younger pre-menopausal AA women who would benefit from early initiationof screening. Finally, the epidemiology and biology of mammographic densities, a risk factor for breast cancer and, perhaps, markers ofaggressive disease require further study in both AA and white women.© 2002 International Society for Preventive Oncology. Published by Elsevier Science Ltd. All rights reserved.

Keywords: African American women; Mammographic screening; Tumor biology; Breast cancer survival

1. Introduction

While breast cancer mortality rates have showed encour-aging decreases among white women during the last decade,by around 1.6% per year, rates for AA women have not de-clined [1]. Breast cancer mortality remains a concern forAA women, at the same time as their rates of participa-tion in mammography screening programs have increased.One possible explanation for this important paradox may bethat the benefits AAs accrue from mammography screen-ing may be less than that for whites[2,3]. This review wasundertaken to elucidate the key issues that may contributeto these disparities, identifying features of mammographyscreening programs and breast cancer biology for AfricanAmerican (AA) women which appear to contribute to theirdiagnoses at more advanced stages than white women, andpoorer long-term prognoses.

∗ Corresponding author. Present address: Department of Epidemiologyand Preventive Medicine, University of Maryland School of Medicine, 401W. Redwood Street, Baltimore, MD 21201, USA. Tel.:+1-410-706-1049;fax: +1-410-706-1050.E-mail address: [email protected] (R. Royak-Schaler).

These disparities remain a national focus, even though thegap in mammography screening observed for AA womenduring the 1980s has been successfully reduced[4,5]. Datafrom the National Health Interview Survey (NHIS) and theBehavioral Risk Factor Surveillance System (BRFSS) doc-ument significant increases in mammography screening forboth AA and white women between 1987 and 1997. Be-tween 1987 and 1990 screening rates rose 23% for AAwomen and 16% for white women; increases for womenliving in households with incomes of<US$ 20,000 rosesimilarly, reaching 24% by 1990[6]. The percentage ofwomen >40 years reporting ever having a mammogram in-creased from 63.9% in 1989 to 84.8% in 1997[5]. Afterage adjustment, those reporting a mammogram within thepast 2 years increased from 54.3% in 1989 to 71.3% in1997.

While these findings suggest progress in screening par-ticipation, AA women remain more likely to be diagnosedwith more advanced stages of breast cancer, and to havepoorer prognoses, than white women[7–9]. This review ad-dresses these important issues, and summarizes and synthe-sizes the findings of research studies which have examined

0361-090X/02/$ – see front matter © 2002 International Society for Preventive Oncology. Published by Elsevier Science Ltd. All rights reserved.PII: S0361-090X(02)00062-4

R. Royak-Schaler, D.P. Rose / Cancer Detection and Prevention 26 (2002) 180–191 181

and compared mammography screening patterns, breast can-cer biology, and cancer outcomes among the study popula-tions of AA and white women.

2. Methods

A search of the MEDLINE and CANCERLIT comput-erized databases was conducted to identify studies whichcompared mammography screening and/or breast cancerbiology in AA and white women. The earliest titles ad-dressing these issues appeared in these databases around1975, and a thorough search was conducted for titles andabstracts between the years 1975 and 2001. The key termsof “mammography screening,” “mammographic density,”“ammographic parenchymal patterns,” “tumor biology,”“interval cancers,” and “ductal carcinoma in situ,” wereused in the literature search. Multiple searches were con-ducted for all terms by using each of the study populationscoupled with a key aspect of mammography screening ortumor biology, e.g. AA and mammographic density. Ref-erence sections of the mammography screening and tumorbiology studies which compared AAs and whites wereexamined for citations not identified in the databases. Ap-proximately 225 abstracts were identified in these searches,and full articles were obtained for those that presentedinformation documenting key components of mammog-raphy screening and tumor biology for AAs and whitesbetween the years of 1975 and 2001. Fifty-five percentof these, 125 studies, were selected for inclusion in thisreview.

Studies were included in this review if: (a) they werepublished in English; (b) discussed racial and socioeco-nomic differences in mammography screening practices,including rates of re-screening; (c) described racial andbody mass differences in mammographic densities andparenchymal patterns; (d) identified racial and socioeco-nomic differences in breast cancer mortality; (e) discussedthe efficacy of screening mammography for women 40–49years old, and those 50 years and over; (f) identified tumorbiology characteristics of breast cancers detected duringscreening and between screenings; and (g) identified tu-mor biology characteristics of breast cancers in AAs andwhites. Overall, it includes studies which examined vari-ables specifically associated with mammography screeningand tumor biology which are predictive of breast canceroutcomes.

This review addresses four key research questions: whatare the features of mammography screening, including den-sities and parenchymal patterns, that correlate with stage ofbreast cancer at diagnosis and survival? What are the op-timal screening intervals for AA and white women to re-duce disparities in stage at diagnosis and survival? Doesequal access to mammography screening influence the rel-ative screening rates and breast cancer outcomes for AAand white women? What is the influence of the biological

characteristics which are known to differ in breast tumorsof AA and white women?

3. Rates of mammography screening and breast cancermortality

A 30% reduction in breast cancer mortality could beachieved if 80% of women ages 50–74 engaged in annualmammography screening[10]. Some studies investigatingannual screening among AA and white women have foundsimilar rates of annual mammography for both groups[11,12]; others have found lower rates for AAs than whites[9,13,14]. Additionally, screening disparities have beennoted for AAs in both primary care and health maintenanceorganization (HMO) settings[9,15–18]. Even with equalaccess to screening in HMOs, AAs seem to receive fewerscreenings than whites.

3.1. Assessing rates of mammography screening

One difficulty in attempting to relate rates of screeningmammography to changes in breast cancer mortality rates,and drawing comparisons between AA and white Amer-ican women, is that different criteria are employed fordefining “use”. These range from “ever had” a mammo-gram[15,19,20], having a mammogram within the last year[19–21], or in the past 2 years[22], to having had a specificnumber of mammograms over a specified period of time[16,23]. When the simplest, but the least relevant, crite-rion of “ever use” was employed, most recent comparisonsfound little difference between AA and white Americanwomen in their exposure to mammography[2,24–27].

To investigate the use of mammography screening amongAA women, The American Cancer Society[28], surveyedself-reported rates of having had a mammogram within thepast 2 or 3 years. It was noted that in 1987 only 19.0% ofwomen aged 50 years or older reported receiving a mammo-gram within 3 years, whereas in 1997 the proportion whohad a single mammogram in the 2-year-period prior to theinterview was 76.1%. While this study found significant in-creases in screening every 2–3 years over the past decade forAAs, this rate may be too infrequent to impact on mortality.McCarthy et al.[23], in a retrospective cohort study, reportedmore advanced breast cancers in AAs compared with whitewomen for those who had not received a screening mam-mogram in the 2 years before diagnosis. AA women whohad received two or more mammograms at least 10 monthsapart were diagnosed with breast cancers that were of sim-ilar stages as whites[18]. This encouraging result suggeststhat regular screening at more frequent intervals may be aneffective approach for reducing late stage diagnosis in AAs.

The most stringent standard for successfully implement-ing a mammography screening program involves identi-fying the proportion of a given population that undergoesrepeated screening during a given period of time. Howe

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[10] concluded that by using the criterion of annual mam-mography screening, a 30% reduction in the breast cancermortality rate could be expected by screening 80% ofwomen aged 50–74 years. But, his survey of 150 womenwith a strong representation of low-income AA patientsfound that only 19% had had two mammograms in a 3-yearstudy period, while 33% ever had had one. Later publica-tions have also described the same low participation of AAwomen in annual mammography screening[27,29].

One obvious concern when evaluating rates of mammog-raphy screening is the reliability of self-reports. Thompsonet al. [30] compared self-reports with hospital records inlow-income women. There was agreement in 82% of caseswhen investigating “ever use” but the actual date of the lastscreening was concordant in only 58% of women. Zapkaet al.[31] studied a large group of ethnically diverse Amer-ican women, and found that 31% reported accurately thetime of their most recent mammogram, and 54% did so towithin 3 months. Greater accuracy was associated with be-ing white, but not with level of education or income. Pre-viously, this same group had reported that in a telephonesurvey of 693 women over 50 years of age, 48% reportedhaving had a mammogram in the last year, but only 20% atleast two recent mammograms at yearly intervals[32]. Inthis study, adherence to the current mammography screen-ing guidelines occurred more frequently in white women,and was associated with higher income, and regular visits toa physician.

3.2. Optimal intervals for mammography screening

Two recurring themes which emerge from the reports ofindividual trials designed to evaluate the efficacy of mammo-graphic screening, and the meta-analyses which they havegenerated, are the influence of duration of observation onthe trial outcome, and the optimal interval between screen-ing which will avoid an unacceptable incidence of new“interval” tumors. Kerlikowske et al.[33] identified 13 stud-ies of the efficacy of mammographic screening, which in-cluded 9 randomized controlled trials and 4 case-controlstudies. While a significant reduction in breast cancer mor-tality was confirmed for screened women aged 50–74 yearswith 7–9 years of follow-up, there was no evidence of ben-efit in those aged 40–49 years and the same follow-up pe-riod. There was a statistically nonsignificant reduction inbreast cancer mortality for women in the 40–49-year groupwho had been followed-up for 10–12 years, but the authorssuggested that sufficient time had elapsed for the onset ofmenopause, and so the screening benefit was not truly per-taining to early-onset disease.

In the Swedish Two-County Trial[34], women in theintervention group aged 40–49 years were screened every2 years, and those aged 50–74 years approximately ev-ery 3 years. Again, in spite of the shorter period betweenscreenings, the effect of screening mammography on thebreast cancer mortality rate was less in the younger women,

due largely to a higher rate of interval cancers. Becauseof the occurrence of rapidly progressing tumors in the40–49-year age group, a screening interval<2 years wasrecommended.

Over the past decade, and despite the failure of the1997 National Institutes of Health Consensus DevelopmentConference to produce a recommendation[35], a strongground swell has developed in the United States in favorof routine annual mammographic screening for womenin the 40–49-year age range. This was encouraged by ameta-analysis of eight randomized controlled trials of mam-mographic screening which involved women who wereaged 40–49 years at entry, and who were followed-up foran average of 12.7 years[36]. A reduction in mortality of18% was observed in the women who received screening,a benefit which was statistically significant. Another studyfocused on prognostic indicators at the time of breast cancerdiagnosis, and differences in overall survival in 971 womenaged 40–49 years according to the mode of detection[37].Mean tumor size was less, and localized disease more fre-quent, in patients whose breast cancers were detected bymammography than those detected by clinical breast exam-ination, breast self-examination, or as an accidental findingby the patient. Moreover, survival was better in patientswith mammography-detected cancers.

There is no evidence that age per se influences the abilityof mammography to detect breast cancer. Rather, it may actas a surrogate for the reproductive hormone activity whichdetermines the presence or absence of structural elementswithin the breast that affect the efficacy of mammographicscreening in modifying detection, and/or disease outcome.It is a basic tenet of the advocacy of mammography-basedbreast cancer screening programs that early detection trans-lates to a more favorable therapeutic outcome. If this is notthe case, detection at an early stage in breast cancer devel-opment, or the identification of tumors which are never des-tined to progress to the invasive/metastatic phenotype, canresult only in patient anxiety, and unnecessary surgical in-tervention. In this context, consideration should be given toreports that mammography is particularly prone to detectcancers with low malignant potential[38–40], as well asductal carcinoma in situ, many of which will never progressto invasive cancer. However, such arguments may evolve,the reverse situation applies to the topic under discussionhere, because we are concerned with the relatively poor out-come of breast cancer in younger women, its associationwith an aggressive phenotype, and the related special caseof AA women. Jones et al.[41] addressed this issue in a re-view of breast cancer survival disparities among AA womenand their relationships to current mammography screeningguidelines presented at the Summit Meeting Evaluating Re-search on Breast Cancer in AA Women. They concluded thatevidence-based strategies were needed to screen AAs underthe age of 50, which could identify in situ carcinomas, andpotentially reduce diagnoses of advanced breast cancer inthis population.

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3.3. Mammography screening and stage at diagnosis inAAs and whites

No randomized controlled trials to date have specificallyassessed the influence of mammography screening on breastcancer survival in AA women. However, some encouragingobservations have been made from data generated by theHealth Insurance Plan (HIP) of Greater New York study.This was the first randomized controlled trial performed inthe United States to determine whether periodic screening bymammography would reduce breast cancer mortality[42].Shapiro et al.[43], having observed the efficacy of screeningin reducing the 10-year follow-up mortality for all womenaged 40–64 years at entry, reanalyzed the data to comparethe screening benefit for AA and white women. The resultsindicated that the poorer prognoses anticipated for AA con-trol women was eliminated among those in the interventiongroup. Because the original design of the HIP trial did nottake racial differences into account, there are several reser-vations about the implications to be drawn from this anal-ysis, and these were discussed by the authors. Two issueswhich merit further consideration are the relative ages ofthe AA and white participants on entry into the trial, andwhether the socioeconomic status of AA women who wereeligible for insurance under HIP, and who took advantage ofthe health plan, were representative of community-dwellingAAs in the United States population.

Other studies have used disease stage at diagnosis asan intermediate marker of outcome in assessing the bene-fit of mammography screening for reducing breast cancermortality in AA women. McCarthy et al.[23] conducted aretrospective cohort study of AA and white breast cancerpatients. They were divided into a control group who hadnot received regular mammographic screening, and an in-tervention group who had been screened on two or moreoccasions during the 2-year period prior to the breast cancerdiagnosis. The AA women were less likely to have under-gone screening, and more likely to have advanced stagedisease at diagnosis. When the women were separated ac-cording to mammography use, the difference in disease stagewas found to be restricted to the non-users. Two potentiallyimportant points about this study are that it was restrictedto women 67 years of age and older, and that “early stage”referred to carcinoma in situ as well as local invasive can-cer, and “later stage” to regional and/or distant metastaticcancer.

Eley et al. [8] did not observe the same equalizationof disease stage as a result of mammography screen-ing. Their population-based investigation included bothpre-menopausal and post-menopausal women with newlydiagnosed breast cancer; 46.2% of the 145 AA, and 30.5%of the 177 white women, were younger than 50 years ofage. The AA patients were diagnosed at later stages ofdisease, and fewer had had a mammogram in the 3 yearsprior to the appearance of symptoms or diagnosis. Partic-ularly noteworthy is that these key differences were most

pronounced in the two groups of women aged 49 years,or younger. However, despite the apparent associations ofrace, disease stage, and use of mammography, this modeof early detection reduced the age-adjusted risk of present-ing with more advanced breast cancer only in the whitewomen.

A small group of studies have focused the on the relation-ships between socioeconomic status, screening, survival,and race. Simon and Severson[9] compared rates of mam-mography screening and stage at diagnosis among AA andwhite women with equal access to screening through HMOs.They initially found that AAs were diagnosed at later stagesof disease than whites, and had lower rates of 5-year sur-vival, 77% compared to 84%. However, the effect of raceon survival diminished after adjusting for stage at diagnosis,income, age, and marital status. A second study conductedwith an HMO population found that white women’s sur-vival remained better than AAs even with equal access toscreening, however, this investigation did not control for so-cioeconomic status[44]. Bassett and Krieger[45] examinedthe effects of sociodemographic factors and stage of diseaseon the association between race and survival. While theyreached similar conclusions to Simon and Severson[9] re-garding the important relationship between socioeconomicstatus and survival rather than race, their population did nothave equal access to screening. This group of studies lendssupport to the need for further investigation of the impor-tant effects of socioeconomic status and stage at diagnosis,as well as race, on breast cancer outcomes for AA women.Other studies support the special significance of tumor bi-ology and its relationship to mammography screening, ascentral for understanding survival disparities among AAscompared to whites.Table 1 presents data from selectedstudies which assessed both stage at breast cancer diagnosisand mammography screening intervals in AA and whitepatients.

4. Tumor biology, early-onset breast cancer, andmammography screening

Breast cancers in AA women have a number of character-istics which are known to predict a poor prognosis in whitewomen[46], and to occur in mammographically detectedcancers with aggressive behavior. In addition to being seenmore often in young, pre-menopausal, women[6,47–51],they are less likely to be steroid hormone receptor positive[6,48,52–54], and more likely to have a higher S-phase frac-tion [48], than do breast cancers in white American women.In addition, the primary tumors from AA breast cancer pa-tients are more often poorly differentiated than those fromwhite patients[5–7,48,53,55].

This difference in tumor biology takes on special signif-icance in the context of mammography screening. Whilethere is almost general agreement that mammography iseffective in reducing the breast cancer mortality rate for


women over 50 years of age, the debate continues re-garding the role, if any, of routine breast screening bymammography in younger women. The arguments in favorof recommending mammographic screening for womenaged 40–49 years[52,53], and against[54,55], have beenpresented in review articles and journal commentaries.These include questions about the validity of the conclu-sions drawn from the published randomized controlledtrials, and the cost-effectiveness of screening women inan age category which contains only approximately 18%of women in the United States who are diagnosed withbreast cancer[56–59]. Also, there are concerns that theemotional burden generated unnecessarily by the false posi-tives which arise from screening this low-risk population isunacceptable.

4.1. Features of breast cancers detected between routinescreenings

True “interval cancers” are those that become symp-tomatic in the interval between screenings, and do notarise in association with a previous false-negative screeningmammogram. In an investigation of the Swedish womenwho had participated in the Malmö mammographic screen-ing trial and who developed interval cancers, a subset wasidentified whose tumors had rapid doubling times; thewomen with these rapidly growing tumors were subse-quently found to have a poor outcome[60]. Tabar et al.[61] refined this observation by showing that the rate of trueinterval cancers was higher in Swedish women aged 40–49years compared with older women, and that this was relatedto the occurrence of more rapidly progressing tumors inthe younger age group. A Dutch study also concluded thatinterval cancers are more common in younger women, andthat they are associated with a high incidence of regionallymph node involvement[62].

In spite of these reports, a debate has emerged as towhether interval breast cancers are truly more aggressive intheir biological behavior, or may be associated with a rel-atively poor prognosis because they can be difficult to rec-ognize by mammographic screening. Of course, these twopossibilities are not mutually exclusive. Ikeda et al.[60]made the interesting observation from the Malmö mammo-graphic screening trial that an excess of medullary and muci-nous carcinomas occurred among interval cancers, and thatthese often had a nonspecific appearance on the mammo-gram performed prior to diagnosis. Similarly, in the SwedishTwo-County Trial not only did a disproportionate number ofinterval cancers occur in younger women, but an unusuallyhigh percentage of these tumors were medullary carcinomas[61].

The relevance of these finding to the present review isthat several groups of investigators have noted that tumorswith medullary histological features occur more frequentlyin AA women[4,48,52–54,63]. However, it seems unlikelythat the higher incidence of medullary cancers is a major

factor in the relatively low impact of mammographic screen-ing among AA women, as this tumor type, although ap-proximately twice as common as in white women, was stillobserved in only approximately 5–6% of cases[48,52,53].

4.2. Mammography and ductal carcinoma in situ

The diagnosis of ductal carcinoma in situ (DCIS), can-cerous epithelial cells which do not invade the surroundingstroma, has undergone a dramatic increase in recent years,due in large part to screening mammography[64–68]. Thereis some inconsistency regarding the reported relative fre-quency of DCIS in AA and white women. Dubin et al.[69]in a case-control study of a mammographically screenedpopulation reported a higher risk for DCIS in AA women,and this was subsequently confirmed by Weiss et al.[70]in a study limited to women aged under 45 years, of whom60% of those with DCIS were identified by routine mam-mography. However, when Simon et al.[71] examined thetime trends from 1973 to 1987 for the diagnosis of CIS, thelargest increase was in black women older than 70 years;in younger AA women, the proportion of total cancers oc-curring as CIS actually decreased over time, and these earlylesions were more often seen in white women. This mayreflect a difference in tumor biology, with a more rapid pro-gression of DCIS to invasive disease in young AA women,and it is also consistent with their earlier onset of clinicallymanifest invasive breast cancer.

There is considerable controversy over the frequencywith which untreated DCIS progresses to invasive breastcancer, and the frequency with which it recurs after surgicalexcision[65,72,73]. Microcalcifications are the most com-mon mammographic manifestation of DCIS, and are asso-ciated with approximately 95% of in situ breast carcinomasdetected by mammography. Moreover, 90% of all cancerspresenting as mammographic microcalcifications are in situlesions, and approximately 80% of these are DCIS[64]. Ithas been reported that linear calcifications, and the linearbranching calcifications which represent central necrosisand the calcification of necrotic material, are particularlyassociated with comedo DCIS, whereas the number anddensity of microcalcifications are not specifically identifiedwith this potentially pre-invasive type of CIS[74,75].

It is evident from this review that there is a deficiencyin the existing mammographic screening programs with re-spect to their ability to identify pre-invasive, potentiallymetastatic, but also potentially curable DCIS. There is alsoa special need for studies designed to investigate the fre-quency with which DCIS is detected in AA women of dif-ferent ages and menopausal status who participate in mam-mographic screening. These investigations should includethe histopathological evaluation and classification of the insitu lesions detected, and the recently developed cellular andmolecular markers which have potential as predictors of sub-sequent biological behavior, and expression of the metastaticphenotype[76].


5. Factors associated with mammographic density inAA and white women

The overall, mammographically defined, breast image isaffected by the amount of adipose tissue present, which isradiolucent, and the connective and epithelial tissues, whichare radiologically dense and appear as white areas on themammogram. Wolfe[77] associated four categories of mam-mographic parenchymal patterns with differing degrees ofbreast cancer risk, the lowest risk occurring in women whosepattern was produced largely by radiolucent fat, and thehighest risk in women with extensive nodular densities (theso-called DY pattern).

More recently, this subjective evaluation has been largelyreplaced by the determination of mammographic densitywhich is expressed as the proportion of the breast volumeoccupied by radiological densities, and for which purposeautomated techniques are now available[78]. In a Canadianstudy, Boyd et al.[79] showed that women with mammo-graphic densities occupying >60–75% of the breast imagewere at four to six times the risk for breast cancer com-pared with those without densities. Later, this same groupdescribed a strong interaction between mammographic den-sity, breast cancer family history, and personal disease risk[80].

5.1. Age and mammographic density

The biological process underlying mammographic den-sity, and its link to breast cancer, has not been fully eluci-dated, but it most likely reflects the level of hormone andgrowth factor-responsive epithelial and stromal prolifera-tion and, perhaps, the degree of new blood vessel forma-tion within the target mammary tissue. Mammographic den-sity is greater in pre-menopausal women, and is increasedduring the luteal phase of the menstrual cycle[81], and inpost-menopausal women by estrogen replacement therapy[82,83]. Plasma insulin-like growth factor-I (IGF-I), whichhas been related to breast cancer risk[80], and, in one asyet unconfirmed study to risk of recurrence in AA patients[84], was found to be positively associated with mammo-graphic density in pre-menopausal women[85]. IGF-I is anangiogenic growth factor, and active angiogenesis in non-cancerous proliferative breast disease and ductal carcinomain situ indicates the potential for progression to invasivecancer[86–88], and has also been associated with a poorprognosis in breast cancer patients[89–91]. Finally, there isalso some evidence that in addition to disease risk, mam-mographic densities may be associated with advanced stage,and with biological markers of a poor prognosis in breastcancer patients[92].

A number of investigators found that the presence ofradiological densities can impair the sensitivity of screen-ing mammography[82,93–96]. One objection to screeningyounger, and by implication pre-menopausal, women is thehigher frequency of mammographically dense breast tissue.

However, in one study the presence or absence of breastdensities did not affect the sensitivity of mammography inwomen younger than 50 years[97], and Feig and cowork-ers[86–98] has argued that technical advances and shorterscreening intervals compensate for this potential handicap.

5.2. Mammographic comparisons in AA andwhite women

Patterson et al.[99] reported a comparison of the mam-mographic features associated with concurrently presentbreast cancer in AA and white women. Overall, there wasno statistically significant difference in the breast parenchy-mal patterns between the two groups, but interpretation ofthe results is made difficult by the variation in factors whichare known to affect mammographic densities. The age ofthe patients varied widely, and unlike the general experienceof age and breast cancer risk, 32% of the white patients, butonly 28% of the AA patients were pre-menopausal. More-over, the potential for misinterpreting the data because ofpost-menopausal estrogen replacement therapy was differ-ent, this being used by 26 (24%) of the white women, butonly 4 (4%) of the AA women.

In contrast to this report are the results of studies de-scribed by Wolfe et al.[100] and, more recently, by Martinet al. [101]. Wolfe et al.[100] in a case-control study de-signed to compare mammographic parenchymal patternsand densities as indicators of breast cancer risk, foundthat mammographic densities involving at least 25% of thebreast “tended” to be more predictive in AA than in whitewomen. The study by Martin et al.[101] involved 425post-menopausal women, 50% of whom were white, and28% AA. None were currently taking hormone replace-ment therapy. In agreement with previous publications, age,gravidity, and body mass index (BMI) were negatively as-sociated with mammographic density. After controlling forage, BMI, smoking, prior hormone replacement therapy, ahistory of hysterectomy, and nulliparity, the highest per-cent mammographic densities were found to occur in AAwomen. However, there was an apparent effect of hysterec-tomy in eliminating the racial difference which may actu-ally have arisen in women who underwent oophorectomywith their hysterectomy, and consequently received ERT.The stimulatory effect of exogenous estrogen on mammarytissue, and density formation, may have obscured the moresubtle endogenous effects associated with ethnicity.

5.3. Obesity and mammographic density

Several studies have found that obesity has an adverse in-fluence on breast cancer prognosis, and that this relationshippersists regardless of menopausal status[102–105]. In gen-eral, AA women are more likely to be overweight than whitewomen[106], and a relatively high incidence of obesity isseen in black breast cancer patients (reviewed by Rose andRoyak-Schaler[46]). Jones et al.[107] found that obesity


was a major contributor to the observed excess risk of moreadvanced disease at the time of diagnosis, and that it wasunrelated to menopausal status.

The mechanism by which obesity influences disease stagemay involve the stimulation of tumor growth and metas-tasis by the accompanying elevation in estrogenic activity[49,108], and, perhaps, angiogenesis. There is, however, anapparent anomaly in the interrelationships between obesity,endocrine changes, and breast tissue as reflected in the fea-tures observed on mammographic examination. Thus, thebiological factors which we have postulated provide themechanism by which obesity exerts its adverse effects onbreast cancer risk and progression are the same as thoseproposed as being responsible for mammographic densities;however, there is uniform agreement that there is aninverserelationship between the BMI and mammographic density[96,101,109–111], such that obese women typically havetranslucent breasts on mammographic examination[110].Moreover, it was reported that although breast density wasstrongly related to a reduction in mammographic sensitivityand an increase in the risk for interval cancers, this was lesscommonly seen in women with high BMIs[96]. The expla-nation may lie in the relative changes in fatty and glandularelements of the breast, with translucent adipose tissue accu-mulating with increasing BMI at a greater rate than do theradio dense epithelial/stromal components. In consequence,the present density would decrease in spite of an absoluteincrease in glandular tissue[111].

Regardless of the complex relationships which exist be-tween obesity, breast physiology, and tumor biology, beingoverweight may have other negative influences on the earlydetection of breast cancer. Size alone might be expected toimpede clinical and self breast examination, and large breastsize was reported to interfere with the mammographic de-tection of cancer[112]. Even so, in the study by Boyd et al.[113] a delay in diagnosis was excluded as the explanationfor the association between obesity and a poor breast can-cer prognosis, and, as already noted, the incidence of inter-val cancers is actually decreased in obese women[96]. Onthe debit side, there is evidence that the presence of obesitycan result in an increased rate of recall for further mammo-graphic investigation and of biopsy[112]. This study, whichwas not analyzed for the influence of race, also found anassociation with larger primary tumors and with metastaticdisease.

Finally, obesity may serve as a potential psychosocialdeterrent to mammography screening. Wee et al.[114]reported that obese patients may be at risk for screeningdisparities which effect breast cancer outcomes. While moreresearch is needed in this area, it seems likely that the roleof health care providers is pivotal in facilitating participa-tion in annual mammography screening by obese women.Communication disparities between AA women and theirhealth care providers have been identified as an importantbarrier to routine early detection[115]. Given the ratesof obesity among AA women, this may be an important

issue for understanding AAs participation in mammographyscreening. Additional research is needed to investigate therelationships among patient obesity, provider communica-tion patterns, and compliance with mammography screeningguidelines.

6. Summary and implications

There is a paucity of data concerning every aspect ofmammography screening in AA women, including an ab-sence of AA-targeted randomized clinical trials upon whichto formulate any evidence-based discussion about screen-ing efficacy. Even though rates of mammography screeninghave increased significantly for AA women since the 1980s,it may be that the nationally recommended guidelines aresuboptimal for their needs given the early onset and aggres-sive nature of their breast cancers, as suggested previouslyby Rose and Royak-Schaler[46] and Jones et al.[41] intheir review presented at the year 2000 Summit EvaluatingResearch on Breast Cancer in AA women.

The important relationships between mammographicscreening histories and tumor biology need clarification.These deficiencies may go a long way in explaining the ob-served increases in breast cancer mortality for AAs whichhave accompanied the overall increases in mammographyscreening.

In 1995, both Feig[116] and Smith [117] defendedthe routine mammography screening of women in the40–49-year age range, and both of these investigators alsostressed the need for shorter intervals between screeningsfor women in this age group[117,118]. However, despitethe advocacy by some investigators the debate over themerits of mammographic screening in women younger than50 years continues, and seems unlikely to be resolved toeveryone’s satisfaction any time soon.

Meanwhile, the past failure to specifically address theearly onset of breast cancer in AA women demands atten-tion. Research is required to determine the importance andpracticality of scheduling mammography during the follic-ular phase of the menstrual cycle[119] and the relativefrequency of interval tumors that occur in AA women ofall ages with both biennial and annual screening schedules,compared to white women. Studies are also required to in-vestigate the tumor biology, including biomarkers of cellproliferation rate and metastatic potential, in screened andunscreened population.

Population-based screening programs for AAs<40 yearsold may be necessary to determine both the optimal ageto begin screening and risk-based screening intervals. Gailand Rimer[120] proposed criteria for the identification ofwomen in the 40–49-year age range whose individual riskwould justify recommending mammographic screening. Theconcept is that all women by age 50 years are likely to ben-efit from, and therefore, are eligible for, routine screening.Further, that this also applies to women in the 40–49 year


age group if, on the basis of a group of specific epidemio-logical and biological risk factors, they are judged to havethe same risk for breast cancer as a 50-year-old woman withno identifiable risk factors.

The model for deriving these risk-based recommendationswas a modification of that originally developed by Gail et al.[121] for white American women, which was employed suc-cessfully in the Tamoxifen Breast Cancer Prevention trial[122]. Gail and Rimer[120] pointed out that for its applica-tion to a mammography screening program separate calcu-lations are required for AA and white women because of thehigher breast cancer incidence in AA women younger than50 years of age, and the likelihood that there are differentialeffects of other risk factors in the two racial groups.

Determining the survival advantages of risk-based mam-mography screening of AA women<40 years old, and theoptimal timing of mammography screening for women withidentifiable risk factors for aggressive interval tumors wouldrepresent important steps in addressing the longstanding dis-parities in breast cancer outcomes for AAs.

Acknowledgements

The authors thank Roz Alexander for assistance in prepar-ing this manuscript.

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Mammography screening and breast cancer biology in African American women—a review