Mammography Screening Behaviors of Women Exposed Prenatally to Diethylstilbestrol

Abstract

Background:

In utero diethylstilbestrol (DES) exposure is a risk factor for rare development of vaginal and cervical cancer and may potentially be a risk factor for breast cancer. Mammography use in this population is relatively unknown; therefore, this study aims to determine if in utero DES exposure is associated with the frequency of mammography screening examinations while considering demographic and clinical factors.

Methods:

Using combined DES cohort questionnaire data, self-reported mammography screening over the past 5 years (2001–2006) was analyzed in women aged ≥45 years. Binary logistic regression assessed if DES exposure was associated with mammography use after adjustment for benign breast disease (BBD), previous cancer diagnosis, and whether insurance access influenced screening use.

Results:

Overall, the frequency of mammography examinations was similar for both DES-exposed and unexposed women. DES-exposed (n=2986) and unexposed women (n=1397) over the age of 44 reported receiving ≥3 mammography examinations in the past 5 years (73.8% and 74.0%, respectively). After adjustment, DES exposure was not associated with ≥3 mammograms in the past 5 years compared to ≤2 examinations (odds ratio [OR] 1.00, 95% confidence interval [CI] 0.86-1.17), p=0.99).

Conclusions:

In utero DES exposure was not associated with mammography use, nor was health insurance status or a BBD or cancer diagnosis. Because of the potential elevated risk for breast cancer in women exposed prenatally to DES, continued monitoring of standard mammography recommendations is recommended for this group, which is predominantly over the age of 45.

Introduction

I n utero diethylstilbestrol (DES) exposure is an established risk factor for the rare development of vaginal and cervical clear cell adenocarcinoma (CCA) in young women.^1
–3 DES is a synthetic estrogen prescribed largely during the 1940s and 1950s to pregnant women to reduce miscarriages and other pregnancy complications. In 1971,^4,5 a strong association was found between CCA and in utero DES exposure in a small group of adolescent females in the New England area.¹ Since then, several nationally funded studies, such as the Diethylstilbestrol Adenosis Project (DESAD), have followed DES-exposed women to identify and describe cervical and vaginal changes in particular but also reproductive and any other changes that might have occurred associated with or influenced by exposure to the drug.⁶ About 0.1%–0.01% of exposed daughters will develop CCA in their lifetime.² In addition, several epidemiologic studies have suggested that prenatally exposed daughters, as well as mothers who took DES during pregnancy, may have an increased risk for breast cancer, possibly by several different mechanisms.^3,5,7,8

Breast cancer rates in the United States have remained constant or have steadily declined in recent years, depending on tumor stage. The Centers for Disease Control and Prevention (CDC) and the National Cancer Institute (NCI) Surveillance, Epidemiology and End Results (SEER) data, collected during the study time frame, report that the rates of in situ cancer in the general population have remained constant during 1999 (28.0/100,000) through 2003 (28.5/100,000) for women of all ages, with Caucasian women having the highest in situ rates of all racial groups.⁹ Conversely, invasive breast cancer rates have steadily declined every year since 1999 (134.0/100,000) through 2003 (119.3/100,000), attributable both to the discontinued use of hormone replacement therapy (HRT) and to increased mammography screening.⁹

Mass mammography screening today is the most useful tool in detecting breast cancer and is the main attributable reason why breast cancer mortality has decreased in women aged 50–69.¹⁰ The U.S. Preventive Services Task Force (USPSTF) reported in 2002 that mammography screening reduced mortality rates by approximately 20% in women >age 50, with a 15% reduction in women aged 40–49.¹¹ Early detection can decrease mortality, prevent the need for aggressive therapy, and improve the outcomes for cosmetic reconstruction. It can be harmful, however, because of the invasiveness of the biopsy procedure and can cause unnecessary psychologic stress.¹²

The early breast cancer screening behavior of women in the DESAD project previously was reported using the frequencies of breast self-examination (BSE), clinical breast examinations (CBE), and mammography based on data collected 17 years ago, when the women were generally in the early to middle reproductive lives.¹³ The results then showed no statistically significant difference between the DES-exposed and unexposed women aged 40–49 in mammography compliance, with both groups reporting 2–3 mammograms in the last 5 years (45% and 44%, respectively).¹³ At that time, only 1% of the DES-exposed and 4% of the unexposed women were≥age 50, which is the age range when women are generally at an increased risk for breast cancer.^9,13 Since then, this population has aged, and new research has shown that these women may be at a potentially higher risk for breast neoplasms than the general population. ^3,5,7,9 To date, the mammography screening behaviors and the factors associated with use are relatively unknown in the DES-exposed population despite this new awareness. Previous population-based studies have found that having access to insurance and healthcare providers, being a younger age, and having reported breast health issues are also factors associated with mammography use.^14

–17

This study aims to determine if there is a difference in mammography use between women>age 45 who were or were not exposed prenatally to DES. Based on previous research, other factors, such as availability of insurance and previous precancerous and cancerous diagnoses, are included to adjust any association between DES exposure and mammography use in this study cohort.

Materials and Methods

Subject recruitment

Data were collected from geographically dispersed national sites: The DESAD project (Boston, MA, Olmsted County, MN, Los Angeles, CA, and Houston, TX); daughters who participated in the Women's Health Study (WHS)(Boston, MA, Dartmouth, NH, and Portland, ME); The Dieckmann Cohort (Chicago, IL); and the Horne Study (Boston, MA). Subjects included in this study were recruited through various methods. The DESAD recruitment methods have been described earlier and required identification of subjects through review of prenatal obstetrics records where DES history was routinely entered, whether in the affirmative or lack thereof. ^2,3,18 Other recruitment methods included enrolling DES-exposed women through physician referral, record review, or walk-in; unexposed women were recruited as siblings of the exposed through record review or by other means.¹⁹ The Dieckmann Cohort recruited in utero DES-exposed and unexposed women whose mothers participated in an DES efficacy clinical trial conducted during the 1950s.⁶ Follow-up of these women began in the 1970s, with questionnaire data collected periodically over the past few decades.⁶ The Horne study included DES-exposed women and unexposed siblings recruited through an infertility specialist's practice over a 20-year period (1952–1972).⁶ Other study participants from both exposure groups came through the WHS by maternal and study subject record review.⁵ Because of the ages for recommendation of mammography, all women analyzed in this study were aged≥45.

Collection of frequency data about mammography use came from self-reporting but, because of resource constraints, was not verified by record review. Responses to the self-administered questionnaires mailed in 2006 were categorized by frequency of mammography examinations (0, 1, 2, and 3 or more times) in the past 5 years (2001–2006). Questionnaire forms were approved by each institution's respective internal review board and the NCI.³

Mammography recommendations during 2000–2006

No specific recommendations about mammography have been made for the in utero DES-exposed population. Mammography guidelines for the general population have varied based on age. During 2002 and earlier, women aged 40–49 were advised to receive a mammogram approximately every 1–2 years, with annual examinations recommended for women aged ≥50.^20,21 Beginning in 2002, the American Cancer Society (ACS), the American Medical Association (AMA), and the American College of Radiology (ACR) moved the age for annual mammography from 50 to 40 years old.²² In addition, in 2002, the USPSTF, The Canadian Task Force on Preventive Health Care (CTFPHC), and the American College of Preventive Medicine (ACPM) recommended mammography screening every 1–2 years starting at age 50.¹¹ The American College of Obstetricians and Gynecologists (ACOG) also recommended a mammogram every 1–2 years for women 40–49 years old and yearly after age 49.¹¹ Further recommendations exist for high risk groups, but are conflicting. In women who are known carriers of the mutated BRCA 1 and 2 genes, the ACS recommends annual mammograms; however, the USPSTF concluded that there is no benefit in increasing screenings and therefore does not have any additional recommendations for this group.²³

As there were several recommendations for mammography screening in women aged ≥45 between 2001 and 2006, it would be difficult to define screening compliance within this group. Therefore, the categorized frequencies of mammography use are reported instead of compliance vs. noncompliance. However, ≥3 examinations were compared to the collapsed ≤2 examinations because the frequency of 3 mammography examinations in the past 5 years approximates 1 mammography examinations every 2 years, which is congruent with most recommendations.

Data analysis

Demographic and medical history factors were compared between the two exposure groups to identify potential confounders for further modeling. The variables of interest included age (continuous variable), race, recruitment site, lack of medical insurance, and a previous diagnosis of benign breast disease (BBD) or any type of cancer. These confounding variables were chosen based on previous research findings and by evaluating whether they changed the effect estimates for DES exposure and other key variables by >10%.^{3,5, 14, 24

–31} Binominal logistic regression was used to determine if DES exposure or any other potential confounders were related to the categorized number of self-reported mammography examination (≥3 compared to ≤2 mammograms). All analyses were calculated using SPSS 19.0 statistical software (SPSS, Inc., Chicago and EpiInfo version 3.5.3).

Results

Descriptive findings

Overall, 2986 DES-exposed and 1397 unexposed women responded to the 2006 questionnaire (87.7% and 90.4%, respectively). Of the aggregate DES-exposed cohorts, 52.5% were recruited through record review, 25.9% through physician referral with documentation of exposure, 18.5% through walk-in appointments, and 3.1% by other methods. Among the unexposed cohorts, 73.0% were recruited through record review, 12.1% were siblings of an exposed woman, and 14.9% were recruited through other means.

In 2006, the mean ages of DES-exposed and unexposed women aged ≥45 were 53.2 years (standard deviation) [SD]±4.0) and 54.5 years (SD±4.6), respectively (Table 1), which was statistically significant by analysis of variance (ANOVA) analysis (p<0.001). There was minimal racial diversity, as nearly all women were Caucasian (exposed 98.2% and unexposed 97.8%), with any single other racial category representing <1% of the total groups. Therefore non-Caucasian study participants were collapsed into one group for comparison analyses. The non-Caucasian group consisted of African Americans, women of Hispanic ethnicity, Asians, and other combined races and ethnicities. There was no association between race and DES exposure (chi-square=0.70, p=0.40). Recruitment sites, categorized by study cohorts, were significantly different among the DES-exposed and unexposed groups (chi-square=547.70, p<0.001). Most participants were members of the DESAD project sites (DES-exposed=82.5%, unexposed=49.8%).

Table 1.

Demographic Characteristics of Diethylstilbestrol-Exposed and Unexposed Women Aged ≥45 Years Who Responded to 2006 Questionnaire (n=4383)

	DES ^a exposed (n =2986)		DES unexposed (n =1397)
	n	%	n	%	Chi-square	p value ^a
Age
Mean (±SD)	53.2 (4.0)	68.1	54.5 (4.6)	31.9	-	<0.001
Race
Caucasian	2930	98.2	1366	97.8
Non-Caucasian^b	55	1.8	31	2.2	0.70	0.40
Recruitment sites^c
Dieckmann Study	194	6.5	174	12.5
WHS	271	9.1	484	34.6
Horne Study	58	1.9	43	3.1
DESAD sites	2463	82.5	696	49.8	547.70	<0.001

p value (2-sided) was derived from ANOVA (age) and the Pearson chi-square analysis.

The non-Caucasian group consisted of African Americans, women of Hispanic ethnicity, Asians, and other combined races and ethnicities.

The locations for the recruitment sites are as follows: Dieckmann Study, Chicago, IL; Women's Health Study (WHS), Boston, MA, Dartmouth, NH, and Portland, ME; Horne Study, Boston, MA; Diethylstilbestrol Adenosis (DESAD) project: Boston, MA, Olmsted County, MN, Los Angeles, CA, and Houston, TX.

SD, standard deviation.

DES was not associated with self-reported diagnosis of cancer, BBD, or lack of health insurance in the unadjusted analysis (Table 2). Overall, both DES-exposed (73.8%) and unexposed (74.0%) women reported having ≥3 mammograms in the past 5 years (2001–2006). The percentages remained >70% even without a BBD or cancer diagnosis. This high percentage of mammography examinations remained in women who did not lack access to care because of insurance status but fell approximately 30% in women who lacked insurance for preventive care in the ≥3 examinations group between the DES-exposed (73.8%–45.5%) and unexposed (74.0%–48.8%) women.

Table 2.

Mammography Use Over 5-Year Period (2001–2006) in Diethylstilbestrol-Exposed and Unexposed Women Aged ≥45 Who Participated in Diethylstilbetrol Study

Mammography use in past 5 Years	DES-exposed (n =2986) n (%)	Unexposed (n =1397) n (%)	Relative risk	95% CI ^a
Two or fewer examinations	752 (26.2)	351 (26.0)
Three or more examinations	2119 (73.8)	997 (74.0)	1.00	0.96-1.04
No care due to lack of insurance
Two or fewer examinations	150 (54.5)	63 (51.2)
Three or more examinations	125 (45.5)	60 (48.8)	0.93	0.75-1.16
Care not affected by insurance status
Two or fewer examinations	572 (22.5)	278 (23.1)
Three or more examinations	1967 (77.5)	927 (76.9)	1.01	0.97-1.05
Had previous BBD diagnosis
Two or fewer examinations	23 (12.8)	5 (6.9)
Three or more examinations	157 (87.2)	67 (93.1)	0.94	0.86-1.02
Did not have previous BBD diagnosis
Two or fewer examinations	729 (27.1)	346 (27.1)
Three or more examinations	1961 (72.9)	930 (72.9)	1.00	0.96-1.04
Had previous cancer diagnosis
Two or fewer examinations	20 (15.3)	7 (12.1)
Three or more examinations	111 (84.7)	51 (87.9)	0.96	0.85-1.09
Did not have previous cancer diagnosis
Two or fewer examinations	732 (26.7)	344 (26.7)
Three or more examinations	2007 (73.3)	946 (73.3)	1.00	0.96-1.04

All p-values nonsignificant at 0.05 level.

BBD, benign breast disease; CI, confidence interval.

Binary logistic regression analysis

The association between DES exposure and ≥3 examinations compared to ≤2 examinations was adjusted using a binary logistic model. The odds ratio (OR) was nonsignificant after adjusting for insurance status, previous BBD, and cancer diagnosis when comparing DES-exposed women and mammography frequency of ≥3 examinations (OR 0.99, 95% confidence interval [CI] 0.86-1.17; p=0.99). Results not shown.

Discussion

Most of the women enrolled in the national DESAD study have since their time of enrollment crossed the time line to being over the age of 45, a time when the risk for developing breast cancer occurs in the general population, which also makes their mammography use a relevant health topic.^5,7 Overall, both DES-exposed (73.8%) and unexposed (74.0%) women reported having ≥3 mammography examinations during the most recent 5-year follow-up period (2001–2006). The percentages remained high even when the women had no known BBD or diagnosed cancer (>70% for ≥3 mammograms). However, percentages fell approximately 30% in the ≥3 examinations group when compared to DES-exposure and stratified by a lack of insurance that prevented routine screening care. This finding is consistent with those of other such studies in the general population.^14

–17 The main factors contributing to mammography use in our cohort were age, previous known BBD, and access to health insurance.

Our cohort's screening behavior frequency, both the DES-exposed and unexposed, is slightly higher when compared to other national surveys. The Behavioral Risk Factor Surveillance System (BRFSS) in 2005 reported 74.6% (95% CI 73.8-75.4) of women aged ≥40 had mammograms in the last 2 years; comparatively, the frequency in our cohort (aged ≥45) was significantly higher (86.8% DES exposed and 87.4% unexposed), each cohort having ≥2 mammograms between 2001 and 2006.¹⁴ In 2010 using 2008 data, BRFSS updated its data of mammography use,²⁴ with 79.9% of women aged 50–59 reporting receiving up-to-date mammograms (i.e., 1 examination in the last 2 years. Our study population has frequencies of >80% for ≥2 examinations, further validating the inference that this cohort's screening behavior is consistently higher than national averages. A possible explanation for our groups' increased screening, whether DES exposed or unexposed, may be attributable to their socioeconomic status, physician compliance, and a priori knowledge of cancer risk (especially as several of the unexposed group are sisters of the exposed, 12.1%); therefore, they have an overall better compliance. To date, the authors are unaware of any thoroughly vetted study that has analyzed the perception of cancer risk in DES-exposed women, but the many newspaper articles, women's magazines, and journals for physicians clearly warn of such possibilities, often subliminally. Previous studies involving the general population have shown that having a relative with breast cancer increases the women's' chance of having a mammogram.^32
–34

The Joint Canada/United States Survey (JCUSH) in 2002–2003 reported that only 68.7% of U.S. women aged 40–69 had at least 1 mammogram within the last 2 years.²⁵ Similarly, in 1997, a cross-sectional survey in Eastern Massachusetts reported that 66% of Caucasian women had a mammogram in the last 2 years.³⁵ When insurance is not a factor, such as with military dependents (71.1% had a mammogram in the last 400 days) or women with universal healthcare access (68.8% adhered to recommendations in Australia), the reported percentages of mammography use resemble the general U.S. population's adherence, with 75% reporting 1 mammogram in the last 2 years in 2005.^14,28,32

Based on our previous studies of breast cancer screening compliance of the 1994 DESAD cohort, DES-exposed women are maintaining compliance to screening recommendations, even when there is no additional clinical risk involced.^13,19 These data showed an overcompliance in CBEs in women without diagnosed BBD (aOR 2.20, 95% CI 1.04-4.67).¹³ Further studies would be useful to understand how DES-exposed women perceive their risk of various cancers, information that well may provide more insight into their reasoning behind compliance with recommended screenings, and to generalize how known familial or environmental predisposition, real or hypothetical, influence women's healthcare decisions.

Our study has several limitations. Mammography screening was not verified through medical chart review. The data presented are self-reported only instead of the gold standard of record review. Self-reported data for mammography screening can be overestimated or underestimated when the reported frequency is validated.^36,37 Self-reporting can also be accurate, with several studies reporting an agreement in mammography screening at 88.4%, with telescoping occurring infrequently (5.7%) in the control groups.^36,37

The second limitation is the inherent bias of being followed in a cancer cohort requiring periodic questionnaires about screening frequency, which may remind participants to seek such testing. Approximately 10% of the unexposed women in this cohort are siblings of women who were exposed in utero to DES and may, therefore, be more aware of cancer screening recommendations, improving their mammography compliance in this cohort analysis.

The DESAD personnel actively attempted to improve response rates from both exposed and unexposed women through telephone calls, web-based access, or mail. Another strength in the design of the DESAD cohort was an initial design to reduce selection bias within its member's recruitment.¹⁹ Medical record abstraction was one of several tools used to recruit the unexposed population. Using medical record review to approach women to participate eliminated important aspects of volunteerism, ideally leading to a more representative sample of the general public to be compared with the DES-exposed group.

Perception of breast cancer health beliefs has a direct effect on behavior in regard to mammography use.²⁹ Personalized views of risk, worry, a family history of breast cancer, and lack of mammography access affect mammography compliance.^33,34 The level of perceived risk also can affect recommended compliance. Curiously, Calvocoressi et al.³⁸ found that women who viewed themselves as having a high risk for breast cancer adhered to guidelines less often than those who viewed themselves as having a moderate risk (aOR 2.83, 95% CI 1.51-5.30), with the effects increasing with age. However, this directly contrasts with our prior work analyzing the original DESAD sites using 1994 data, which found women without a BBD diagnosis overly complied with CBE policy.¹³ These results may have been a result of the overall age of the cohort, who were predominantly<age 50.

Another motivating factor in mammography use is physician recommendation.^30,31,39 It is not known how often gynecologists recommend mammograms to women exposed in utero to DES. It is known that nearly all (98%) physicians are aware of the breast cancer guidelines,⁴⁰ yet one study showed that physicians do not inform one fourth of their female patients about routine mammography screening guidelines.³⁹ Surprisingly, primary care physicians are more likely than gynecologists to recommend mammography screening for women in their 50's.³⁹

Conclusions

Overall, DES-exposed and unexposed women are receiving regular mammography examinations (≥3 mammograms within a 5-year period). Although DES exposure as a specific variable is not a significant factor in complying with mammography screening policy, mammography remains important because the frequency of breast cancer is so high for all women in general. Attention to mammography compliance should improve the chances of detecting a breast neoplasm, particularly in light of the potential for increased breast cancer development in the DES-exposed group.

Footnotes

Disclosure Statement

The authors have no conflicts of interest to report.

References

Herbst

, Ulfelder

, Poskanzer

. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med, 1971; 284:878–881.

Hatch

, Palmer

, Titus-Ernstoff

et al. Cancer risk in women exposed to diethylstilbestrol in utero. JAMA, 1998; 280:630–634.

Troisi

, Hatch

, Titus-Ernstoff

et al. Cancer risk in women prenatally exposed to diethylstilbestrol. Int J Cancer, 2007; 121:356–360.

Federal Food and Drug Administration Bulletin. Diethylstilbestrol contraindicated in pregnancy. Washington, DC: U.S. Department of Health, Education, and Welfare, 1971.

Palmer

, Wise

, Hatch

et al. Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol Biomarkers Prev, 2006; 15:1509–1514.

Hatch

, Herbst

, Hoover

et al.

Incidence of squamous neoplasia of the cervix and vagina in women exposed prenatally to diethylstilbestrol (United States)

Cancer Causes Control, 2001; 12:837–845.

Palmer

, Hatch

, Rosenberg

et al.

Risk of breast cancer in women exposed to diethylstilbestrol in utero: Preliminary results (United States)

Cancer Causes Control, 2002; 13:753–758.

Wacholder

, Hartage

, Prentice

et al. Performance of common genetic variants in breast-cancer risk models. N Eng J Med, 2010; 362:986–993.

Centers for Disease Control and Prevention. Decline in breast cancer incidence—United States, 1999–2003. MMWR, 2007; 56:549–553.

10.

Elmore

, Armstrong

, Lehman

, Fletcher

. Screening for breast cancer. JAMA, 2005; 293:1245–1256.

11.

U.S. Preventive Services Task Force. Screening for breast cancer: Recommendations and rationale. Ann Intern Med, 2002; 137:344–346.

12.

Ringash

. Canadian Task Force on Preventive Health Care. Preventive health care, 2001 update: Screening mammography among women aged 40–49 years at average risk of breast cancer. Can Med Assoc J, 2001; 164:469–476.

13.

Camp

, Coker

, Troisi

et al. Breast cancer screening in women exposed in utero to diethylstilbestrol. J Womens Health, 2009; 18:547–552.

14.

Centers for Disease Control and Prevention. Use of mammograms among women aged ≥40 years—United States, 2000–2005. MMWR, 2007; 56:49–51.

15.

Phillips

, Kerlikowske

, Baker

, Chang

, Brown

. Factors associated with women's adherence to mammography screening guidelines. Health Serv Res, 1998; 33:29–42.

16.

Swan

, Breen

, Coates

, Rimer

, Lee

. Progress in cancer screening practices in the United States: Results from the 2000 National Interview Survey. Cancer, 2003; 97:1528–1540.

17.

Selvin

, Brett

. Breast and cervical cancer screening: Sociodemiographic predcitors among white, black, and Hispanic women. Am J Public Health, 200; 93:618–623.

18.

Jefferies

, Robboy

, O'Brien

et al. Structural anomalies of the cervix and vagina in women enrolled in the diethylstilbestrol adenosis (DESAD) project. Am J Obstet Gynecol, 1984; 148:59–66.

19.

Camp

, Coker

, Troisi

et al. Cervical screening and general physical examination behaviors of women exposed in utero to diethylstilbestrol. J Lower Genital Tract Dis, 2008; 12:111–117.

20.

American College of Obstetricians and Gynecologists. Committee opinion: Committee on Gynecologic Practice. Diethylstilbestrol. Int J Gynecol Obstet, 1994; 44:184.

21.

Moore

. A survey of state Medicaid policies for coverage of screening mammography and Pap smear services. Womens Health Inst, 1992; 2:40–49.

22.

Green

, Taplin

. Breast cancer screening controversies. J Am Board Fam Pract, 2003; 16:233–241.

23.

Robson

, Offit

. Management of an inherited predisposition to breast cancer. N Eng J Med, 2007; 357:154–162.

24.

Centers for Disease Control and Prevention. Vital signs: Breast cancer screening among women aged 50–74 years—United States, 2008. MMWR, 2010; 59:813–816.

25.

Blackwell

, Martinez

, Gentleman

. Women's compliance with public health guidelines for mammograms and Pap tests in Canada and the United States. Womens Health Issues, 2008; 18:85–99.

26.

Shin

, Schneider

, Cole

, Laronga

. Follow-up recommendations for benign breast biopsies. Breast J, 2006; 12:413–417.

27.

Miedema

, Tatemichi

. Breast and cervical cancer screening for women between 50 and 69 years of age: What prompts women to screen? Womens Health Issues, 2003; 13:180–184.

28.

Amin

, Shriver

, Henry

, Lenington

, Peoples

, Stojadinovic

. Breast cancer screening compliance among young women in a free access healthcare system. J Surg Oncol, 2008; 97:20–24.

29.

Katapodi

, Lee

, Facione

, Dodd

. Predictors of perceived breast cancer risk and the relation between received risk and breast cancer screening: A meta-analytic review. Prev Med, 2004; 38:388–402.

30.

Schueler

, Chu

, Smith-Bindman

. Factors associated with mammography utilization: A systematic quantitative review of the literature. J Womens Health, 2008; 17:1477–1498.

31.

Legg

, Fauber

, Ozcan

. The influence of previous breast cancer upon mammography utilization. Womens Health Issues, 2003; 13:62–67.

32.

Antill

, Reynolds

, Young

et al. Screening behavior in women at increased familial risk for breast cancer. Fam Cancer, 2006; 5:359–368.

33.

Hay

, McCaul

, Magnan

. Does worry about breast cancer predict screening behaviors? A meta-analysis of the prospective evidence. Prev Med, 2006; 42:401–408.

34.

Cohen

. Breast cancer early detection, health beliefs, and cancer worries in randomly selected women with and without a family history of breast cancer. Psychooncology, 2006; 15:873–883.

35.

David

, Ko

, Prudent

, Green

, Posner

, Freund

. Mammography use. J Natl Med Assoc, 2005; 97:253–261.

36.

Norman

, Localio

, Zhou

et al. Validation of self-reported screening mammography histories among women with and without breast cancer. Am J Epidemiol, 2003; 158:264–271.

37.

Caplan

, McQueen

, Qualters

, Leff

, Garrett

, Calonge

. Validity of women's self-reports of cancer screening test utilization in a managed care population. Cancer Epidemiol Biomarkers Prev, 2003; 12:1182–1187.

38.

Calvocoressi

, Kasl

, Lee

, Stolar

, Claus

, Jones

. A prospective study of perceived susceptibility to breast cancer and nonadherence to mammography screening guidelines in African American and white women ages 40 to 79 years. Cancer Epidemiol Biomarkers Prev, 2004; 13:2096–2105.

39.

Dominick

, Skinner

, Bastian

, Bosworth

, Strigo

, Rimer

. Provider characteristics and mammography recommendation among women in their 40s and 50s. J Womens Health, 2003; 12:61–71.

40.

Zapka

, Puleo

, Taplin

et al. Breast and cervical cancer screening: Clinicians' views on health plan guidelines and implementation efforts. J Natl Cancer Inst Monogr, 2005; 35:46–54.