Barriers Related to Mammography Use for Breast Cancer Screening Among Minority Women

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Barriers Related to Mammography Use for Breast Cancer Screening Among Minority Women Irene Alexandraki, MD, MPH; Arshag D. Mooradian, MD

Purpose: The purpose of this review was to better understand possible social, economic, cultural, behavioral, and systems barriers to breast cancer screening among minority women. Methods: Relevant manuscripts were identified through a MEDLINE/PubMed search for English-language literature from October 1971 through April 2009. The abstracts from a total of 515 manuscripts were reviewed. Only studies conducted among minority women in the United States and examining barriers related to screening mammography were considered. Of 64 relevant articles, 13 cross-sectional and 4 prospective studies met inclusion criteria. Study design; patient characteristics; outcomes regarding knowledge, attitudes and beliefs; social norms; accessibility; and cultural competence regarding breast cancer screening were abstracted. Studies were rated using a methodological quality score (MQS). Results: Pain and embarrassment associated with screening mammography, low income and lack of health insurance, poor knowledge about breast cancer screening, lack of physician recommendation, lack of trust in hospitals and doctors, language barriers, and lack of transportation were the most frequently identified barriers. The average MQS of the studies selected was 10.9 (SD = 3.25, range, 4-20). Conclusions: Multiple barriers limit screening mammography among minority women. Recognizing predictors of screening among minority women and addressing culturally specific barriers may improve utilization of screening mammography among these women. Keywords: breast cancer n screening n minority n women’s health J Natl Med Assoc. 2010;102:206-218 Author Affiliations: From the Department of Medicine, University of Florida College of Medicine, Jacksonville, Florida. Correspondence: Irene Alexandraki, MD, MPH, FACP, Department of Medicine, University of Florida, 653-1 West Eighth St, Jacksonville, FL. 32209 ([email protected]).

INTRODUCTION

A

pproximately 1 in 8 women will develop breast cancer during her lifetime, making breast cancer the most common noncutaneous malignancy among women in the United States. Recent estimates indi206 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION

cate that there were more than 211 000 new cases and more than 40 000 deaths as a result of breast cancer among women in 2005. Considerable resources are devoted to research, disease control efforts, and screening in particular.1,2 Reduction in mortality from breast cancer depends on successful interventions aimed at early detection and treatment. Screening mammography can diagnose breast cancer at an early stage, often before a lump is felt by the woman or on clinical breast examination. The percentage of women diagnosed with breast cancer after screening mammography ranges from 4% to 7%.3 Breast cancer does not occur in all racial and ethnic groups equally. The latest data from the Surveillance, Epidemiology, and End Results program show a higher incidence of breast cancer among Caucasian women (141.1/100 000 women) compared with African American (119.4), Asian/Pacific Islander (96.6), Hispanic (89.9), and American Indian/Alaska Native (54.8) women. However, breast cancer mortality is higher among African American women (34.7 deaths /100 000 women) compared with Caucasian women (25.9 deaths/100 000).In addition, the 5-year survival among African American, Hispanic, and American Indian/Alaska Native women also trails that of Caucasian women.4-7 To date, women such as Native Americans/Alaska Natives, Hispanics, women of lower socioeconomic backgrounds and in rural areas, uninsured women and those without a usual source of care, women over age 70, and recent immigrants have not achieved the Healthy People 2010 objective of 70% participation in mammography within the prior 2 years. Although disparities in screening mammography have improved overall since the early 1990s, significant differences in screening persist among many medically underserved communities and minority women.8 This review systematically examines and organizes findings from available studies regarding barriers in the use of mammography for breast cancer screening among minorities in the United States. The principal aim from this review is to understand the possible social, economic, cultural, behavioral, and systems barriers to breast cancer screening care among minority women in the United States. The observations derived from this systematic review will be useful in developing strategies to address some of the health care disparities in this country. VOL. 102, NO. 3, MARCH 2010

Barriers to mammography among minority women

METHODS Data Sources and Searches Relevant manuscripts were identified through a MEDLINE/PubMed search for English-language literature from October 1971 through April 2009. The key phrases used included breast cancer screening, barriers, minorities, racial differences, ethnicity, mammography, breast cancer, minority women, poverty, rural, underserved, cultural beliefs, mammography utilization, and low income. Only manuscripts that had full text available online were selected.

Study Selection For inclusion in the review, studies had to (a) be published in a peer reviewed, English-language journal; (b) be conducted in the United States; (c) examine the barriers related to mammography use for breast cancer screening; (d) include minority women; (e) use statistical analysis methodology for their data evaluation, including content and thematic analysis. Exclusion criteria included (a) commentaries, systematic reviews, or other nonresearch studies on the topic; (b) non–peer reviewed publications; (c) non–English-language publications; (d) publications not accessible online; (e) studies not conducted in the United States; (f) studies on genetic testing and counseling in breast cancer; (g) studies on screening tests after diagnosis of breast cancer. The studies that were reviewed but excluded are summarized in Table 1. The MEDLINE/PubMed search using the key phrases outlined in Methods identified a total of 515 manuscripts. Scanning these articles’ abstracts resulted in 64 relevant studies, from which only 17 (13 cross-sectional and 4 prospective studies) met our inclusion criteria. The majority of these studies (16 of 17 included) were qualitative. The reviewed studies were conducted in various settings and minority populations, and their results varied in the focus, methods, results and conclusions. Outcomes regarding knowledge, attitudes and beliefs; social network experience; accessibility; and cultural competence regarding breast cancer screening among minority women in the United States were examined.

Data Extraction and Quality Assessment A review matrix was created to structure the information abstracted from each study (Table 2). This matrix allowed the authors to abstract information on study design, sample characteristics, data collection methods, measurement instruments, data validity and reliability, statistical techniques employed in data analyses, study findings and conclusions, and overall methodological quality score.9 The data collection focused on barriers related to mammography use for breast cancer screening exclusively. If the studies measured both barriers and facilitators related to screening mammography, only information regarding barriers was collected. In addition, if the study examined barriers related to other screening modalities (eg, breast self-examination) or cancers (eg, cervical cancer screening), those data were not collated. Each individual study was rated using a methodological quality score (MQS). The rating was determined by using the set of criteria developed by Bernstein10 and described by Patton.11 The criteria for the MQS included assessments of the design of each study, theory use (or not use), sample size and characteristics, the use of previously tested measures, testing and reporting of the validity of study data and reliability, level of sophistication of the analytical techniques, as well as use of statistical controls when determining the association between barriers and screening mammography use among minority women. For each of these criteria, a numbered score was given to the reviewed study if it contained the specific elements defined for each dimension. Twenty was the maximum score a study could achieve when all criteria were used.12 The barriers identified in this review were organized into categories based on the theory of reasoned action (TRA) and theory of planned behavior (TPB). This selection was made based on the fact that they offer a theoretical framework that identifies personal attitudes (eg. knowledge and belief about efficacy of screening), subjective norms (eg, influence of significant others, social influence), and perceived behavioral control (eg, accessibility).13,14

RESULTS

Seventeen studies met our inclusion/exclusion criteria. Thirteen studies (76.4%) were cross sectional (Table 3).

Table 1. Summary of Excluded Studies and Reasons for Exclusion (n = 47) Barriers were not addressed.29,41-50 Full-text online version was not available.51-58 Focus was the evaluation of breast cancer screening programs.59-64 There were barriers to follow-up (not screening) after an abnormal screening mammogram.65-67 Studies had been conducted in countries other than the United States.68-73 Studies included participants with breast cancer.74-78 There were barriers to genetic breast cancer counseling.79 Systematic reviews39,80-82 Letter to the editor83 Commentary84 Minority women were not included.85

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None of the reviewed studies had a retrospective design and only 1 was exclusively quantitative. The majority of the studies were conducted in the northeastern and midwestern United States, with the largest number of them (n = 14) published in the last 10 years (after 1998). Eight studies had large samples of more than 300 participants. Age and ethnicity were reported in all the studies. African American, Hispanic, Asian American, Pacific-Islander

(including Filipino American), and Native American women were considered minorities. Only 1 study was conducted among Amish and Appalachian women.15 Twelve of the 17 studies included African American women. In 1 study, minority was defined by income (≤200% of poverty threshold) and not by race.16 One-on-one interviews and focus groups were the preferred methods for data collection in the majority of the reviewed studies (88%).

Table 2. Matrix of 17 Reviewed Studies Examining Barriers Related to Mammography Use for Breast Cancer             Authors

Methods

Barriers

Burnett et al, 199531

Study: Cross-sectional Participants (n = 339): ≥40 y, African American (90%), Hispanic (6%), uninsured, without a PCP (38%), low income Data collection: interviews Measurement instrument: designed by authors Theory: Theory of Reasoned Action

Having an uncaring health care practitioner (ie, nurses, physicians), procedure too lengthy

Dibble et al, 199719

Study: Cross-sectional Participants (n = 597): ≥18 y, African American, Asian American, Caucasian, Hispanic and Pacific Islander, able to write and read English Data collection: in-clinic interviews Measurement instruments: a demographic questionnaire and the Attitude Toward Breast Cancer Screening Procedures scale Theory: Theory of Reasoned Action

Fear and embarrassment about the procedure and its results, language barrier, lack of time, pain during mammo, concern and fear about radiation exposure, beliefs about susceptibility to breast cancer

Champion Study: Prospective longitudinal intervention (3 data et al, 199727 collections over a year) Participants (n = 328): 45-64 y, African American, low income Data collection: in-home interviews Measurement instrument: developed by authors Framework: Behavioral Model for Health Services Utilization Theory: health belief model

Lack of regular physician; lack of PCP’s recommendation; not thinking about mammo; poor knowledge about mammo and breast cancer

Skinner et al, 199823

Age ≥ 75 y, lack of knowledge about breast cancer screening, lower education level, lack of regular medical care and unfamiliarity with available resources, fear of cancer diagnosis, patient at a private physician office, lack of physician recommendation, pain and embarrassment associated with the procedure

Study: Qualitative cross-sectional Participants (n = 253): ≥ 60 y (mean, 72.5 y), African American (88%), low income, less than eighthgrade education (38%) Data collection: telephone or in-person interviews Measurement instrument: “standard protocol” Theory: health belief model, and transtheoretical model

Bailey et al, Study: Qualitative 200026 Participants (n = 60): ≥ 40 y (median: 50 y), African American, low income, high school degree or less (66%) Data collection: focus groups Measurement instrument: questionnaire based on the Witness Project86 Framework: Witness Role Model by Erwin86 (theorybased cancer education program for African American women) Theory: health belief model

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Misconceptions about cancer, confidence in nontraditional cancer treatments, fears about disease’s impact on personal relationships, cultural perception on breast cancer screening

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Table 4 summarizes the barriers related to mammography use for breast cancer screening among minority women as encountered in the reviewed studies. These findings were organized in 3 sections based on the TRA and TPB framework: patients’ attitudes and beliefs, accessibility and associated factors, and social influence. The most frequently identified barriers in these studies were related to women’s attitudes and beliefs.

Personal Attitudes and Beliefs The pain and embarrassment associated with screening mammography were identified as barriers in the 10 out of the 17 studies (58.8%).15,17-25 In the study by Husaini et al, rural women tended to report more barriers and considered that a mammogram would be embarrassing, while none of the urban women did (p = .009).20 Dibble et al found that African American women had a

Screening Among Minority Women (Studies Presented in Chronological Order) Results

Conclusions

Intention to have a mammo was positively related to a significant other’s influence (p = .01), one’s attitude towards mammo (p = .54), a caring relationship with a health care practitioner

Need for breast cancer screening programs that encourage involvement of significant others and provide a respectful environment for patient interaction

13

African Americans had a more positive attitude toward breast cancer screening than Asian American (p < .002), Caucasian (p < .05), Hispanic (p < .001), or Pacific Islander (p < .002) women; Hispanic women were more embarrassed about mammo than African American or Caucasian women.

Addressing culturally specific concerns regarding breast cancer screening is imperative

16

Women were more likely to be compliant with screening mammo if they perceived fewer barriers and more benefits, and had more knowledge about the disease.

The role of a health care provider in recommending mammo is important; addressing culturally specific barriers and establishing consistency in PCPs may improve breast cancer screening

18

Overall barrier scores were highest for precontemplators (p < .001), but contemplators were most likely to worry about finding a lump (p < .05).

Knowledge is associated with mammography contemplation; barriers may affect whether contemplation leads to action; precontemplators may need explanation of the rationale for breast cancer screening and contemplators interventions to assuage fears.

16

The Witness Project program increased women’s knowledge and reduced fears about cancer and encouraged them to seek breast cancer information; 67% of this program’s participants had a mammo after completing the program

The once perceived cultural barriers can actually be applied as a cultural intervention strategy to improve breast cancer screening designed specifically for African American women

11

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more positive attitude toward breast cancer screening procedures, while Hispanic women had significantly more embarrassment associated with mammography than did either African American or Caucasian women.19 Poor knowledge about breast cancer screening and the risk factors associated with cancer was found to be a barrier in 6 studies (35.2%).17,21,23,25-27 In the study by Ko et al, lack of information on breast cancer screening guidelines was a barrier among Filipino American women.28 Only 32% of the African American and Native American women surveyed in Paskett’s study could answer correctly at what age

a woman should begin receiving mammograms.29 Personal attributes such as physical symptoms, family history, and knowledge about breast cancer could serve either as a motivator or barrier to breast cancer screening for this ethnic group in the study by Wu.25 When Chinese women were surveyed by Su et al, only 46% of them reported knowing about mammograms, while only 37% believed that a mammogram was the most effective breast cancer early detection method.30 Tejeda et al showed that Mexican women aged 50 years and over believed that they need a mammogram only when they feel pain or a lump on their breast.24

Table 2. Matrix of 17 Reviewed Studies Examining Barriers Related to Mammography Use for Breast Cancer             Authors

Methods

Barriers

Bernstein et Study: Qualitative cross-sectional al, 200018 Participants (n = 151): ≥ 50 y, African American (75%), Caucasian, Hispanic and Haitian Data collection: brief motivational interview followed by a telephone survey Measurement instrument: structured interviews Theory: Roger’s Protection Motivation Theory, transtheoretical model

Lack of transportation and time, fear of what might be found, cost, pain associated with mammo, family responsibilities, lack of trust in hospitals and doctors, embarrassment associated with mammo, language barrier, complexity of the mammo registration process

O’Malley et Study: Qualitative cross-sectional al, 200216 Participants (n = 1,205) : ≥ 40 y, low income (30%), African American (82%), Caucasian, and Hispanic Data collection: household telephone survey Measurement instrument: surveys Theory: None

Lack of continuity and coordination of care, lack of comprehensive services, not being in a private health maintenance organization, lack of patient-clinician trust and communication

Ko et. al, 200328

Study: Qualitative cross-sectional Participants (n survey = 248, n focus group = 58), 20-77 y, Filipino American Data collection: surveys and focus group Measurement instrument: not reported Theory: health belief model

Lack of time and transportation, lowincome, fear of finding cancer, language barrier, not wishing to think about getting a mammo and perception that it’s not important, embarrassing to discuss, lack of information (focus group)

Ahmed et al, 200417

Study: Qualitative cross-sectional Participants (n =25): ≥40 y, African American and Caucasian, low income, ≤12th-grade education (8%), positive family history of breast cancer (28%) Data collection: focus groups Measurement instrument: not reported Theory: precede-proceed model

Lack of awareness and knowledge of risk factors, lack of trust in the treatment and screening process, lack of personal responsibility for health, lack of pride in self, chance of finding cancer, discomfort of the procedure, overconfidence produced by a “null finding”

Paskett et al, 200422

Study: Experimental design (random sample) Participants (n = 892: >40 y, Caucasian, African American and Native American Data collection: survey Measurement instrument: not reported Theory: None

Lack of time and health insurance, lack of encouragement from physician, family or friend, embarrassment, difficulty accessing resources, perception of low personal breast cancer risk, exposure to radiation, poor knowledge, pain associated with mammo

Husaini et al, 200520

Study: Qualitative pilot study Participants (n = 326): ≥40 y, African American, urban and rural samples Data collection: in-home interviews Measurement instrument: not reported Theory: None

Not thinking about getting a mammo, lack of doctor recommendation, perception that mammo is unnecessary as “breasts are healthy”, perception that mammo is embarrassing, religious beliefs, pain associated with mammo

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Bernstein et al reported that only 35% of women aged 50 years and over knew that they were at higher risk for breast cancer, and 65% of them never had a mammogram.18 In the study by Ahmed et al, the number and types of screening tests was an inhibiting factor that could become overwhelming, depressing, and stressful among women older than 40 years.17 However, age was not identified as a barrier in Burnett’s study, which was conducted among English-speaking African American and Hispanic women.31 There were significant differences by ethnicity in the beliefs concerning the likelihood of getting breast cancer

(p < .005), with Pacific Islander women reporting that they were significantly more likely than African American (p < .004) or Caucasians (p < .005) to get breast cancer.19 Lack of trust in hospitals and doctors was identified as another barrier in 5 studies (29.4%).16-18,31,32 Patientphysician relationship was extremely important for African American, Asian, and Hispanic women in deciding whether to follow their physicians’ recommendations. Their opinions about racial and ethnic concordance with their physicians and importance of their doctors’ credentials differed among these groups.32

Screening Among Minority Women (Studies Presented in Chronological Order) (cont) Results

Conclusions

Mammo underutilization was exhibited among the participants; 66% of women followed up and 60% had a postintervention mammo; >90% of women planned to repeat mammo next year; 77% of women who did not have a mammo requested a “second try” appointment

Respecting and allowing patient to express her own ideas about mammo and providing her with advice, feedback, and practical assistance may increase screening mammo utilization.

10

65% of respondents were adherent to breast cancer screening; coordination of care was associated with screening adherence but only for women age ≥65.

Organizing services to promote continuity with a specific PCP and better patient-practitioner relationships may improve adherence to breast cancer screening among minority women.

12

Lack of time was the most frequently reported barrier to participation in breast cancer screening; participants showed high reliance and trust in the health information provided by PCP and the media.

There is need to assess Filipino women’s cultural and demographic variables to better assess how this group’s cultural and socioeconomic background affects their health behavior.

9

Awareness and knowledge of risk factors, trust in the health care process, attitudes of personal responsibility, preventive health care–seeking actions, and an internal reward system of pride and satisfaction contributed to overcoming barriers to breast cancer screening.

The partnering of women who are positive about prevention with those who are nonadherent may prove an important element for increasing the level of mammo adherence among minority women.

7

24% of participants had never received a mammogram; 2/3 of them had not been recommended a mammo by their physicians; Native American and African American women had less knowledge, more inaccurate beliefs, and barriers to breast cancer screening compared with Caucasian women.

Low-income women are in need of encouragement to be screened and of information regarding opportunities to obtain mammo.

10

Rural women tended to report more barriers to mammo screening than the urban women; only women from the rural sample (16.2%) thought that a mammo would be embarrassing.

Education programs might need to be adapted according to the population of interest; faith communities may have a potential role in facilitating programs to educate rural women about breast cancer screening.

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Accessibility and Associated Factors The second most frequently identified group of barriers in these studies was related to accessibility and associated factors (Table 4). Seven of the 17 studies identified low income and lack of health insurance as barriers to screening mammography.15,23,25,28-30,32 Moy and colleagues found major difficulties arising when a woman was between jobs and without medical insurance for a period of time.32 In the study by Tejeda et al, women of Mexican

descent older than 50 years who had never had a mammogram mentioned the cost of the examination, lack of time, and health insurance as barriers.24 Lack of knowledge about insurance coverage created a significant barrier for Filipino women interviewed by Wu et al.25 Difficulty in accessing services was identified as another barrier. Lack of transportation was identified in 4 studies (23.6%)15,18,21,28 and was a paramount issue among African American, Appalachian, and Amish women in the study by

Table 2. Matrix of 17 Reviewed Studies Examining Barriers Related to Mammography Use for Breast Cancer             Authors

Methods

Barriers

Ogedegbe Study: Qualitative cross-sectional et al, 200521 Participants (n = 187): 50-69 y, African American (44%), Hispanic (51%), ≥12th grade (39%), low income (92%) Data collection: in-depth one-on-one interviews Measurement instrument: not reported Theory: precede-proceed

Competing priorities, pain from procedure, lack of cancer screening knowledge, embarrassment and low selfefficacy for the procedure, perception of good health, family discouragement, lack of medical recommendation, cost of test, lack of transportation, language barrier

Wu & Bancroft, 200625

Study Qualitative study Participants (n = 11): 45-80 y (mean, 56.9 y), Filipino American Data collection: focus groups (3 sessions) Measurement instrument: developed by authors Theory: none

Cultural beliefs in sharing information about cancer, lack of family support and recommendation from PCP, lack of health insurance and pain related to the procedure, difficulties in accessing health service

Moy et al, 200632

Study Qualitative study Participants (n = 49): >40 y (median, 49 y), African American, Asian American, and Hispanic Data collection: focus groups Measurement instrument: developed by authors Theory: theory of planned behavior and attitudesocial influence-efficacy model

Competing priorities (financial strain, domestic violence, and drug abuse), health beliefs, community perspectives, lack of trust in their physician, lack of health insurance, language barrier, negative prior experience

Su et al, 200630

Study: Qualitative cross-sectional Participants (n = 111): 24-70 y, Chinese, education >12 y (22.9%), low income (66%) Data collection: translated questionnaire Measurement instrument: developed by author Theory: None

Inability to afford medical care, lack of insurance, language barrier, not knowing where to get medical care, lack of breast symptoms, cost of mammo

Documet Study: Qualitative et al, 200815 Participants (n = 312 women and 168 providers), median age: African American: 33.5 y, Amish: 42 y, Appalachian: 47 y, Hispanic: 29 y; low income Data collection: 2 focus groups; mail surveys and in person or via follow-up interviews with providers Measurement instrument: Not reported Theory: social ecology and precede model

Noncompliance with PCP recommendations, feeling intimidated during appointments, misinformation about breast cancer screening, language barrier, limited literacy, fear of breast cancer and death, pain associated with the procedure, lack of health insurance, unfamiliarity with appointment scheduling, cost, lack of transportation

Tejeda et al, Study: Qualitative 200924 Participants (n = 40): ≥50 y, Mexican descent Data collection: in-home individual interviews Measurement instrument: social network index by Suarez87 Theory: none

Lack of health insurance, lack of physician recommendation, perceived low risk for breast cancer, lack of knowledge about prevention, cost, lack of time off from work, pain associated with the exam, fear of finding breast cancer, not knowing others with cancer

Abbreviations: mammo: mammogram; MQS: Methodological Quality Score (based on study design, theoretical framework, sample size and

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Documet et al.15 Difficulty to schedule an examination, forgetfulness about a scheduled mammography appointment, and unfamiliarity with and concerns about the number of questions asked during the mammography registration process were some of the barriers identified.18,25 In the study by Bernstein at al, for women age 50 and over, childcare for grandchildren was a common barrier, while time off from work was rarely an issue.18 For Asian women interviewed by Moy et al, time off from work

was a prohibitive factor for getting mammograms, while for African American women, financial strain, domestic violence, and drug abuse were competing issues that made breast cancer screening less important.32 Language barriers and translation problems were identified as barriers in 5 studies (29.4%).18,19,28,30,32 Hispanic, Haitian, Chinese, and Pacific Islander (including Filipino) women were found to have more inadequate English proficiency,15,18,19,28,30 while Skinner et al identified an education

Screening Among Minority Women (Studies Presented in Chronological Order) (cont) Results

Conclusions

MQS

The most commonly barrier was the perception of not needing the test due to good health or an absence of symptoms attributable to ill health; fear of pain was the most common reason for not planning to have a future mammo.

Patients’ attitudes and beliefs, their social network experience, and accessibility of services may serve as a useful framework for PCP’s to educate and counsel their patients about cancer screening behaviors.

8

Support from family members, PCP recommendations, health insurance reinforcement, and personal attributes of physical symptoms, family history, and health literacy are facilitators of Filipino American women’s screening practices.

There is a need to address the cultural, social, and health care system factors related to breast cancer screening in Filipino American women.

7

Lack of insurance was not a barrier for African American and Hispanic women. Mammorelated embarrassment, language barrier, and factors in physician preference were different among the 3 groups.

Health interventions to improve breast cancer screening among minority women may be more successful if they address group-specific concerns.

8

71% of women ≥40 y had a prior mammo; having a PCP as information source of mammo (p = .002) was a significant predictor of having ever had a mammo.

Chinese women remain a largely underserved minority population, especially in regard to cancer screening and treatment.

11

First-person narratives can be good instruments Group screening may be a culturally appropriate 10 for delivering accurate information about breast strategy for organizing breast cancer screening cancer risks and tests. for Amish, Hispanic and African American women; clinical cultural competence can assist health care providers in improving communication with patients.

Knowing people with cancer, talking to their daughters about their health and being part of a social network facilitated breast cancer screening. Time in the United States is a more important factor for screening than the size of the social network. Reaching women in smaller groups or in a one-on-one setting may be more effective for screening promotion interventions than widespread media messages.

Daughters and female relatives of Mexican women may be useful channels for screening promotion interventions.

8

characteristics, measurement instrument, data validity and reliability testing, and analytical techniques); PCP: primary care physician.

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level less than 12th grade as a barrier.23 Limited literacy made it difficult for African American, Amish, and Appalachian women to understand any medical pamphlets they might receive in the study by Documet et al.15 Asian and Hispanic participants interviewed by Moy et al expressed preference to have a physician who spoke their native language and could relate to their culture.32

Social Influence The third most frequently identified barriers in these studies were related to social influence (Table 4). In the study by Paskett et al, 67% of all women reported that their physician had never encouraged them to receive a mammogram, although 75% reported having received a regular checkup in the preceding year.29 In contrast, Moy et al showed that most women knew their recommended schedule for mammograms and agreed that their primary care physicians were appropriately recommending it.32

African American, Amish, and Appalachian women in the study by Documet et al stated that they did not always follow their providers’ recommendations and often felt too intimidated to ask questions during visits.15 The role of culture as a barrier to screening mammography was noted in 3 studies.20,25,26 In the study by Moy et al, fatalistic beliefs that a breast cancer diagnosis would inevitably lead to death was a prominent reason for African American women to generally avoid screening mammograms. These beliefs resulted from their personals experiences recalling “friends and family who had died shortly after being diagnosed with breast cancer.”32 Documet et al reported that Appalachian women tended to live isolated in smaller communities and lacked opportunities for connecting with each other, although Amish women were highly active within their social network despite their little contact outside their communities.15 In Filipino culture, avoidance was the major theme

Table 3. Methodological Criteria and Frequency Distribution of Each Criterion Among 17 Reviewed Studies Examining Barriers Related to Mammography Use for Breast Cancer Screening Among Minority Women Methodological Characteristic Study design

Scoring Options Cross-sectional design = 1 point Retrospective design = 2 points Prospective design = 3 points Theoretical framework The study had no theory = 0 points for quantitative studies The study was based on an implicit theory = 1 point The study was based on a specific theory = 2 points Theoretical framework The study neither built a theory nor linked its findings to a for qualitative studies specific theory = 0 points The study linked its findings to a specific theory = 1 point The study developed a theory = 2 points Sample size Small sample (<100) = 1 point Medium sample (>100 and < 300) = 2 points Large sample (>300) = 3 points Age Not reported = 0 points Reported = 1 point Ethnicity Not reported = 0 point Reported = 1 point Measurement instrument Not reported = 0 point Authors developed the instrument measuring barriers = 1 point Authors adopted a previously established instrument measuring barriers = 2 points Data validity testing Not reported = 0 points Reported = 1 point Data reliability testing Not reported = 0 point Reported = 1 point Data analysis Qualitative analysis (content and thematic analysis) = 1 point Univariate statistics/descriptive = 1 point Bivariate statistics/ANOVA = 2 points Multiple/logistic regression/ANCOVA = 3 points Multivariate statistics (structural equation modeling) = 4 points Barriers for breast No barriers were identified = 0 points cancer screening Uncontrolled analysis (factors were not tested for statistical significance) = 1 point Controlled analysis (factors were tested for statistical significance) = 2 points

Frequency (n) 13

% 76.4

4 1

23.6 5.9

5 11

29.4 64.7

5 4 8

29.4 23.6 47

17

100

17 6 5 6

100 35.3 29.4 35.3

13 4 13 4 7 3 1 4 2

76.4 23.6 76.4 23.6 41.2 17.6 5.9 23.6 11.7

9 8

53 47

Abbreviation: ANCOVA, analysis of covariance.

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in dealing with a cancer diagnosis. Furthermore, Wu et al reported that unspoken traditions and beliefs made these women uncomfortable with touching or exposing their bodies or talking about their breasts.25 For Mexican women in Tejeda’s study, having a social network was not associated with prior mammogram screening.24 Community advocacy was a key motivator for African American, Asian American, and Hispanic women to continue breast cancer screening in the study by Moy et al.32 Advice from family and friends (and, most importantly, from health care professionals), family history of cancer, knowing someone with cancer, and exposure to health promotion encouraged African American and Hispanic women to undergo cancer screening as reported by Ogedegbe at al.21

Methodological Quality The methodological quality of the reviewed studies varied. The average MQS was 10.9 (SD = 3.25), within a theoretical range of 4 to 20 points. Most reviewed studies comprised cross-sectional designs (76.4%), and almost half (47%) examined large (>300 participants) samples. All except for 1 study were qualitative, and 64.7% of the studies linked their findings to a specific theory. Seven of the qualitative studies (41%) used content and thematic analysis, while 9 out of 16 used mixed methodology for the interpretation of their results. Among the studies that employed a theoretical framework, 3 studies used the TRA and TPB (17.6%), 4 used the health belief model (23.6%), 2 were based on the transtheoretical model constructs (11.8%), while 3 (17.6%) applied the precede-proceed framework to guide their inquiry. Four studies (23.6%) applied 2 different theories concurrently (Tables 2 and 3).

DISCUSSION

The use of a theoretical framework to organize findings from various studies offers an advantage over traditional systematic reviews. The theory identifies both the constructs and the logical connections among them and can facilitate causal thinking and knowledge development. The use of theoretical categories also helps identify which factors are overrepresented or underrepresented in the body of literature under review.33 According to the TRA, the intention to participate in screening for breast cancer is determined primarily by 2 factors: the woman’s attitude toward breast cancer screening procedures and the social normative influence of the people who are important in her life.13 The TRA is built on the assumption that most of the behaviors are under volitional control, an assumption that is not true for all behaviors. To overcome the weakness of the model, Ajzen13 introduced the construct of perceived behavioral control or the TPB. This theoretical framework is appropriate to study breast cancer screening for 2 reasons: (1) the TPB allows for an understanding of the cultural perspectives affecting the behavior, JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION

and (2) mammography screening behavior is not fully under volitional control because it is influenced by environmental factors; thus, perceived behavioral control becomes a valuable theoretical construct.14 Using the TRA/TPB framework, 19 factors that were identified as barriers to screening mammography in minority populations were organized into 3 categories: personal attitudes and beliefs, social influence, and factors related to accessibility and availability of resources. Pain and embarrassment associated with the mammogram were the most frequently identified barriers and were mentioned by 10 studies.15,17-25 Furthermore, in certain cultures such as Chinese American, women’s issues of modesty and shyness may preclude breast cancer screening. Fear or anxiety towards mammography may relate to poor knowledge or to the woman’s first experience with the test.34 Community-based breast cancer education programs, such as the Witness Project Program,26 may increase women’s knowledge and reduce fears about cancer and encourage them to seek screening. Providing women with information prior to the mammogram may reduce the pain or discomfort that the women experience during the examination.35 Educational programs and materials should be relevant to the needs of the women who identify with a particular cultural or ethnic group. For underserved populations, tailored messages in an interactive format such as in-person or individualized counseling have been shown to be more effective at increasing mammography rates (10.7% to 19.9%) compared to nontailored interventions such as pamphlets (2.7% to 3.5%).36 The value of social ties for certain ethnic groups such as African American and Hispanic women should not be overlooked, as they have shown to influence health behaviors.37 In a context where ethnic minorities interact less frequently with formal health services and often distrust the health care system, community health educators should overcome the social, linguistic, and cultural barriers to mammography. The once-perceived cultural barriers can actually be applied as a cultural intervention strategy to improve breast cancer screening designed specifically for these women. Health literacy is increasingly recognized as a critical factor affecting communication across the continuum of care, including screening. Low literacy may also influence the source and accuracy of the information received. All these factors may, in turn, influence participation in cancer screening.38 Recent research has highlighted illiteracy as an independent contributor to cancer disparities.39 Lack of trust in hospital and doctors resulted in mammography underutilization.16-18,31,32 Often, cultural discordance between physician and patient may cause a communication gap and lead to mistrust. Health care educators and providers with an understanding of cultural norms could better reach underserved women. This approach will build a foundation of trust between the health care provider and the patient and may lead to an VOL. 102, NO. 3, MARCH 2010 215

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increased participation in cancer screening programs. The lack of physician recommendation for a mammogram was the most frequently identified social barrier to screening mammography regardless of ethnicity. Educational approaches to primary care professionals may change mammography-prescribing behaviors and increase breast cancer screening among minority populations. A meta-analysis by Mandelblatt showed that interventions to change provider behavior were effective and increased mammography use from 6% to 21%.40 The lack of continuity and coordination of care among minorities may further contribute to the disparities in the delivery of preventive care including breast cancer screening among medically underserved women. Furthermore, low income, lack of health insurance and cost of mammogram, lack of resources, language barrier, and lack of time and transportation were barriers to screening mammography among minority women. Providing transportation and translation services, and facilitating scheduling may assist women to overcome the logistical barriers to mammography. Providing free or low-cost mammography in nonthreatening settings such as churches and community centers may increase use of screening mammography in these populations. It is noteworthy that there are limitations in the present review. This search strategy only included full-text articles available online and might have missed any studies not indexed in the MEDLINE/PubMed database or only in print. All the reviewed studies were conducted in the

United States. In addition, not all ethnic minority groups were included in these studies. The use of a single theoretical framework based on TRA and TPB to organize findings of studies that might have used a different theoretical model has some limitations. However, the TRA/ TRB framework deemed the most appropriate to study breast cancer screening for the reasons mentioned above. The overall quality of the studies reviewed appears to be fair based on the mean MQS of 10.9. The criteria for developing the MQS favored rigorous, experimentaltype designs and might not have rendered the best fit for qualitative studies with focus on individuals’ choices and behaviors. Another limitation is the evaluation process and ranking of the identified barriers. The conclusions drawn may have some inherent weaknesses due to the qualitative design and thematic analysis of the majority of the studies in the literature.

CONCLUSION

Despite limitations, this review highlights the barriers to screening mammography use among minority women in the United States. Developing culturally sensitive breast cancer education and screening programs is necessary. Negative personal attitudes, experiences and beliefs towards mammography, lack of access and resources, communication barriers, lack of physician recommendation and discouragement from family and friends were all barriers to screening mammography among minority women. In contrast, previous positive personal experience from mammog-

Table 4. Barriers to Mammography Use for Breast Cancer Screening Among Minority Women Identified in the Reviewed Articles Barriers I. Personal attitudes and beliefs Pain and embarrassment associated with procedure Fear of positive mammogram result Lack of knowledge about breast cancer screening and/or cancer itself Lack of knowledge about mammogram and its advantages Lack of trust in hospital and doctors Perception of being healthy Concerns and fear about radiation exposure Perception that mammogram is not important II. Accessibility and associated factors Low income and lack of health insurance Lack of resources and information about their availability Cost of mammogram Language barrier Lack of time Lack of transportation Complexity of registration process for mammography Lower educational level III. Social Influence Lack of physician recommendation for mammogram Lack of encouragement; discouragement from others Cultural role

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References 15,17-25 17-19, 21, 23, 24, 28 17, 21, 23, 25-27 15, 17, 22, 23, 27 16-18, 31, 32 21, 24, 30, 32 19, 21, 22 20, 28 15, 16, 15, 18, 18, 15, 15, 23

22, 22, 18, 19, 19, 18, 18

24, 23, 21, 28, 22, 21,

25, 25, 24, 30, 24, 28

28, 30, 32 28, 30 30 32 28

20, 22 - 25, 27 21, 22, 25, 32 20, 25, 26

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raphy, positive influence from family or friends, a caring relationship with a health care practitioner, trust in the health care process, awareness and knowledge about screening practices and benefits facilitated breast cancer screening. Recognizing predictors of screening among minority women, addressing culturally specific barriers, establishing consistency in primary care providers, and increasing confidence and knowledge through education may improve utilization of screening mammography among minority women. Designing and implementing programs that could build cultural competency skills among physicians may better reach underserved communities. Future studies should focus on demonstrating culturally appropriate interventions in the realms of policy, health care provision, and clinician training.

References

1. Blackman DJ, Masi CM. Racial and ethnic disparities in breast cancer mortality: are we doing enough to address the root causes? J Clin Oncol. 2006;24(14):2170-2178. 2. Smigal C, Jemal A, Ward E, et al. Trends in breast cancer by race and ethnicity: update 2006. CA Cancer J Clin. 2006;56(3):168-183. 3. Eheman CR, Benard VB, Blackman D, et al. Breast cancer screening among low-income or uninsured women: results from the National Breast and Cervical Cancer Early Detection Program, July 1995 to March 2002 (United States). Cancer Causes Control. 2006;17(1):29-38. 4. Jemal A, Murray T, Ward E, et al. Cancer statistics, 2005. CA Cancer J Clin. 2005;55(1):10-30. 5. Wolf AB, Brem RF. Decreased mammography utilization in the United States: why and how can we reverse the trend? AJR Am J Roentgenol. 2009;192(2):400-402. 6. Li CI. Racial and ethnic disparities in breast cancer stage, treatment, and survival in the United States. Ethn Dis. 2005;15(2 suppl 2):S5-9. 7. Vernon SW, Tilley BC, Neale AV, Steinfeldt L. Ethnicity, survival, and delay in seeking treatment for symptoms of breast cancer. Cancer. 1985;55(7):1563-1571. 8. HP2010. Cancer - Goals. http://www.healthypeople.gov/document/ html/volume1/03cancer.htm#_Toc490540731. Accessed April 5, 2009. 9. Garrard J. Health Sciences Literature Review Made Easy: the matrix method. 2nd Edition. Jones and Bartlett Publishers, MA: Sudbury, 2007. 10. Bernstein I, Freeman HE. Academic and entrepreneurial research: consequences of diversity in federal evaluation studies: New York, NY: Russell Sage; 1975. 11. Patton M. Utilization-focused evaluation: the new century text, 3rd ed.: Thousand Oaks, CA: Sage Publications; 1997. 12. Suther S, Goodson P. Barriers to the provision of genetic services by primary care physicians: a systematic review of the literature. Genet Med. 2003;5(2):70-76. 13. Ajzen I. Understanding attitudes and predicting social behaviors: Englewood Cliffs, NJ: Prentice-Hall; 1980. 14. Tolma EL, Reininger BM, Evans A, Ureda J. Examining the theory of planned behavior and the construct of self-efficacy to predict mammography intention. Health Educ Behav. 2006;33(2):233-251. 15. Documet PI, Green HH, Adams J, Weil LA, Stockdale J, Hyseni Y. Perspectives of African American, Amish, Appalachian And Latina women on breast and cervical cancer screening: implications for cultural competence. J Health Care Poor Underserved. 2008;19(1):56-74. 16. O’Malley AS, Forrest CB, Mandelblatt J. Adherence of low-income women to cancer screening recommendations. J Gen Intern Med. 2002;17(2):144-154. 17. Ahmed NU, Fort JG, Elzey JD, Bailey S. Empowering factors in repeat mammography: insights from the stories of underserved women. J Ambul Care Manage. 2004;27(4):348-355. 18. Bernstein J, Mutschler P, Bernstein E. Keeping mammography referral

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION

appointments: motivation, health beliefs, and access barriers experienced by older minority women. J Midwifery Womens Health. 2000;45(4):308-313. 19. Dibble SL, Vanoni JM, Miaskowski C. Women’s attitudes toward breast cancer screening procedures: differences by ethnicity. Womens Health Issues. 1997;7(1):47-54. 20. Husaini BA, Emerson JS, Hull PC, Sherkat DE, Levine RS, Cain VA. Ruralurban differences in breast cancer screening among African American women. J Health Care Poor Underserved. 2005;16(4 suppl A):1-10. 21. Ogedegbe G, Cassells AN, Robinson CM, et al. Perceptions of barriers and facilitators of cancer early detection among low-income minority women in community health centers. J Natl Med Assoc. 2005;97(2):162-170. 22. Paskett ED, Tatum C, Rushing J, et al. Racial differences in knowledge, attitudes, and cancer screening practices among a triracial rural population. Cancer. 2004;101(11):2650-2659. 23. Skinner CS, Arfken CL, Sykes RK. Knowledge, perceptions, and mammography stage of adoption among older urban women. Am J Prev Med. 1998;14(1):54-63. 24. Tejeda S, Thompson B, Coronado GD, Martin DP. Barriers and facilitators related to mammography use among lower educated Mexican women in the USA. Soc Sci Med. 2009;68(5):832-839. 25. Wu TY, Bancroft J. Filipino American women’s perceptions and experiences with breast cancer screening. Oncol Nurs Forum. 2006;33(4):E71-78. 26. Bailey EJ, Erwin DO, Belin P. Using cultural beliefs and patterns to improve mammography utilization among African-American women: the Witness Project. J Natl Med Assoc. 2000;92(3):136-142. 27. Champion V, Menon U. Predicting mammography and breast selfexamination in African American women. Cancer Nurs. 1997;20(5):315-322. 28. Ko CM, Sadler GR, Ryujin L, Dong A. Filipina American women’s breast cancer knowledge, attitudes, and screening behaviors. BMC Public Health. 2003;3:27. 29. Paskett ED, Tatum CM, Mack DW, Hoen H, Case LD, Velez R. Validation of self-reported breast and cervical cancer screening tests among low-income minority women. Cancer Epidemiol Biomarkers Prev. 1996;5(9):721-726. 30. Su X, Ma GX, Seals B, Tan Y, Hausman A. Breast cancer early detection among Chinese women in the Philadelphia area. J Womens Health (Larchmt). 2006;15(5):507-519. 31. Burnett CB, Steakley CS, Tefft MC. Low-income, minority women. Barriers to cancer screening. Ann N Y Acad Sci. 1995;768:277-280. 32. Moy B, Park ER, Feibelmann S, Chiang S, Weissman JS. Barriers to repeat mammography: cultural perspectives of African-American, Asian, and Hispanic women. Psychooncology. 2006;15(7):623-634. 33. Chen LS, Goodson P. Factors affecting decisions to accept or decline cystic fibrosis carrier testing/screening: a theory-guided systematic review. Genet Med. 2007;9(7):442-450. 34. Mo B. Modesty, sexuality, and breast health in Chinese-American women. West J Med. 1992;157(3):260-264. 35. Miller D, Livingstone V, Herbison P. Interventions for relieving the pain and discomfort of screening mammography. Cochrane Database Syst Rev. 2008(1):CD002942. 36. Yabroff KR, O’Malley A, Mangan P, Mandelblatt J. Inreach and outreach interventions to improve mammography use. J Am Med Womens Assoc. 2001;56(4):166-173, 188. 37. Kang SH, Bloom JR, Romano PS. Cancer screening among AfricanAmerican women: their use of tests and social support. Am J Public Health. 1994;84(1):101-103. 38. Davis TC, Williams MV, Marin E, Parker RM, Glass J. Health literacy and cancer communication. CA Cancer J Clin. 2002;52(3):134-149. 39. Peek ME, Han JH. Disparities in screening mammography. Current status, interventions and implications. J Gen Intern Med. 2004;19(2):184-194. 40. Mandelblatt JS, Yabroff KR. Effectiveness of interventions designed to increase mammography use: a meta-analysis of provider-targeted strategies. Cancer Epidemiol Biomarkers Prev. 1999;8(9):759-767. 41. Lovejoy NC, Jenkins C, Wu T, Shankland S, Wilson C. Developing a breast cancer screening program for Chinese-American women. Oncol Nurs Forum. 1989;16(2):181-187. 42. Rimer BK. Interventions to increase breast screening. Lifespan and ethnicity issues. Cancer. 1994;74(1 suppl):323-328.

VOL. 102, NO. 3, MARCH 2010 217

Barriers to mammography among minority women 43. Sheinfeld Gorin S, Gemson D, Ashford A, et al. Cancer education among primary care physicians in an underserved community. Am J Prev Med. 2000;19(1):53-58. 44. Meade CD, Calvo A, Rivera M. Screening and community outreach programs for priority populations: considerations for oncology managers. J Oncol Manag. 2002;11(5):20-28. 45. Otero-Sabogal R, Owens D, Canchola J, Golding JM, Tabnak F, Fox P. Mammography rescreening among women of diverse ethnicities: patient, provider, and health care system factors. J Health Care Poor Underserved. 2004;15(3):390-412. 46. Maxwell AE, Bastani R, Vida P, Warda US. Strategies to recruit and retain older Filipino-American immigrants for a cancer screening study. J Community Health. 2005;30(3):167-179. 47. Gorin SS, Ashford AR, Lantigua R, et al. Effectiveness of academic detailing on breast cancer screening among primary care physicians in an underserved community. J Am Board Fam Med. 2006;19(2):110-121. 48. Ferrante JM, Chen PH, Jacobs A. Breast and cervical cancer screening in obese minority women. J Womens Health (Larchmt). 2006;15(5):531-541. 49. Brown Sofair J, Lehlbach M. The role of anxiety in a mammography screening program. Psychosomatics. 2008;49(1):49-55. 50. Bastani R, Kaplan CP, Maxwell AE, Nisenbaum R, Pearce J, Marcus AC. Initial and repeat mammography screening in a low income multiethnic population in Los Angeles. Cancer Epidemiol Biomarkers Prev. 1995;4(2):161-167. 51. Caplan LS, Wells BL, Haynes S. Breast cancer screening among older racial/ethnic minorities and whites: barriers to early detection. J Gerontol. 1992;47 Spec No:101-110. 52. Roetzheim RG, Van Durme DJ, Brownlee HJ, Herold AH, Woodard LJ, Blair C. Barriers to screening among participants of a media-promoted breast cancer screening project. Cancer Detect Prev. 1993;17(3):367-377. 53. Gotay CC, Issell BF, Hernandez BY, Serxner S. Barriers to mammography in a low income, multiethnic clinic population. Hawaii Med J. 1996;55(8):136-140. 54. Valdini A, Cargill LC. Access and barriers to mammography in New England community health centers. J Fam Pract. 1997;45(3):243-249. 55. Thompson B, Montano DE, Mahloch J, Mullen M, Taylor V. Attitudes and beliefs toward mammography among women using an urban public hospital. J Health Care Poor Underserved. 1997;8(2):186-201. 56. Reding DJ, Lappe KA, Krueger M, Kolehouse BL, Steneil D, Leer RA. Cancer screening and prevention in rural Wisconsin: the Greater Marshfield Experience. Wis Med J. 1997;96(8):32-37. 57. Rawl SM, Champion VL, Menon U, Foster JL. The impact of age and race on mammography practices. Health Care Women Int. 2000;21(7):583-597. 58. McGarvey EL, Clavet GJ, Johnson JB, 2nd, Butler A, Cook KO, Pennino B. Cancer screening practices and attitudes: comparison of low-income women in three ethnic groups. Ethn Health. 2003;8(1):71-82. 59. McCoy CB, Smith SA, Metsch LR, et al. Breast cancer screening of the medically underserved: results and implications. Cancer Pract. 1994;2(4):267-274. 60. Yu MY, Seetoo AD, Hong OS, Song L, Raizade R, Weller AL. Cancer screening promotion among medically underserved Asian American women: integration of research and practice. Res Theory Nurs Pract. 2002;16(4):237-248. 61. Jibaja-Weiss ML, Volk RJ, Kingery P, Smith QW, Holcomb JD. Tailored messages for breast and cervical cancer screening of low-income and minority women using medical records data. Patient Educ Couns. 2003;50(2):123-132. 62. Gellert K, Braun KL, Morris R, Starkey V. The ‘Ohana Day Project: a community approach to increasing cancer screening. Prev Chronic Dis. 2006;3(3):A99. 63. Gany FM, Shah SM, Changrani J. New York City’s immigrant minorities. Reducing cancer health disparities. Cancer. 2006;107(8 suppl):2071-2081. 64. Freund KM, Battaglia TA, Calhoun E, et al. National Cancer Institute Patient Navigation Research Program: methods, protocol, and measures. Cancer. 2008;113(12):3391-3399.

218 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION

65. Rojas M, Mandelblatt J, Cagney K, Kerner J, Freeman H. Barriers to follow-up of abnormal screening mammograms among low-income minority women. Cancer Control Center of Harlem. Ethn Health. 1996;1(3):221-228. 66. Yabroff KR, Washington KS, Leader A, Neilson E, Mandelblatt J. Is the promise of cancer-screening programs being compromised? Quality of follow-up care after abnormal screening results. Med Care Res Rev. 2003;60(3):294-331. 67. Wujcik D, Fair AM. Barriers to diagnostic resolution after abnormal mammography: a review of the literature. Cancer Nurs. 2008;31(5):E16-30. 68. Bell TS, Branston LK, Newcombe RG, Barton GR. Interventions to improve uptake of breast screening in inner city Cardiff general practices with ethnic minority lists. Ethn Health. 1999;4(4):277-284. 69. Meana M, Bunston T, George U, Wells L, Rosser W. Older immigrant Tamil women and their doctors: attitudes toward breast cancer screening. J Immigr Health. 2001;3(1):5-13. 70. Wollin J, Elder R. Mammograms and Pap smears for Australian deaf women. Cancer Nurs. 2003;26(5):405-409. 71. Thomas VN, Saleem T, Abraham R. Barriers to effective uptake of cancer screening among Black and minority ethnic groups. Int J Palliat Nurs. 2005;11(11):562, 564-571. 72. Remennick L. The challenge of early breast cancer detection among immigrant and minority women in multicultural societies. Breast J. 2006;12 Suppl 1:S103-110. 73. Brotto LA, Chou AY, Singh T, Woo JS. Reproductive health practices among Indian, Indo-Canadian, Canadian East Asian, and Euro-Canadian women: the role of acculturation. J Obstet Gynaecol Can. 2008;30(3):229-238. 74. Maly RC, Leake B, Silliman RA. Health care disparities in older patients with breast carcinoma: informational support from physicians. Cancer. 2003;97(6):1517-1527. 75. Ashing-Giwa KT, Padilla G, Tejero J, et al. Understanding the breast cancer experience of women: a qualitative study of African American, Asian American, Latina and Caucasian cancer survivors. Psychooncology. 2004;13(6):408-428. 76. Carlson LE, Angen M, Cullum J, et al. High levels of untreated distress and fatigue in cancer patients. Br J Cancer. 2004;90(12):2297-2304. 77. Hurd TC, James T, Foster JM. Factors that affect breast cancer treatment: underserved and minority populations. Surg Oncol Clin N Am. 2005;14(1):119-130, vii. 78. Ell K, Sanchez K, Vourlekis B, et al. Depression, correlates of depression, and receipt of depression care among low-income women with breast or gynecologic cancer. J Clin Oncol. 2005;23(13):3052-3060. 79. Halbert CH, Kessler LJ, Mitchell E. Genetic testing for inherited breast cancer risk in African Americans. Cancer Invest. 2005;23(4):285-295. 80. Consedine NS, Magai C, Krivoshekova YS, Ryzewicz L, Neugut AI. Fear, anxiety, worry, and breast cancer screening behavior: a critical review. Cancer Epidemiol Biomarkers Prev. 2004;13(4):501-510. 81. Loerzel VW, Bushy A. Interventions that address cancer health disparities in women. Fam Community Health. 2005;28(1):79-89. 82. Masi CM, Blackman DJ, Peek ME. Interventions to enhance breast cancer screening, diagnosis, and treatment among racial and ethnic minority women. Med Care Res Rev. 2007;64(5 suppl):195S-242S. 83. Kachroo S. Pharmacists should assume a larger role in overcoming the racial/ethnic barriers to breast cancer screening. J Manag Care Pharm. 2006;12(5):406-407. 84. Bigby J. Global understanding of barriers to breast cancer screening. J Womens Health (Larchmt). 2006;15(5):484. 85. Nash D, Chan C, Horowitz D, Vlahov D. Barriers and missed opportunities in breast and cervical cancer screening among women aged 50 and over, New York City, 2002. J Womens Health (Larchmt). 2007;16(1):46-56. 86. Erwin DO, Spatz TS, Stotts RC, Hollenberg JA, Deloney LA. Increasing mammography and breast self-examination in African American women using the Witness Project model. J Cancer Educ. 1996;11(4):210-215. 87. Suarez L, Lloyd L, Weiss N, Rainbolt T, Pulley L. Effect of social networks on cancer-screening behavior of older Mexican-American women. J Natl Cancer Inst. 1994;86(10):775-779. n

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