Abstract
Background:
The U.S. Preventive Services Task Force (USPSTF) does not recommend routine mammogram screening for women aged 40–49 years at average risk for breast cancer. We aimed to assess the extent to which women were following guideline recommendations and to examine whether guideline awareness and other individual-level factors were associated with adherence.
Materials and Methods:
We surveyed a nationally representative panel of 383 U.S. women aged 40–49 years at low risk for hereditary breast cancer in October 2019.
Results:
Only 29% of women reported not having initiated screening mammography. Most women (80%) were unaware of the USPSTF screening guideline related to age of initiation and frequency of mammography. Being aware of the recommendation to initiate screening at age 50 increased the odds of not initiating screening (odds ratio [OR] = 6.70, p < 0.001), whereas being older than 45 years (OR = 0.22, p < 0.001) and having a primary care doctor decreased the odds of not initiating screening (OR = 0.25, p < 0.001).
Conclusions
: Mammogram screening in excess of USPSTF recommendations is prevalent among U.S. women aged 40–49 years. Efforts are needed to increase women's awareness of the rationale for guidelines and the opportunities to discuss with providers whether delaying mammograms is appropriate.
Introduction
Controversy surrounding the age to initiate and the appropriate interval for mammography screening has been ongoing for at least two decades. Evidence-based guidelines now endorse tailoring mammogram screening to a woman's individual risk profile (e.g., age, genetics, family cancer history) through use of validated risk models. 1,2 The U.S. Preventive Services Task Force (USPSTF) updated its mammogram screening guideline in 2009 and now does not recommend routine screening mammography for average risk women between the ages of 40 and 49 years (henceforth referred to as de-implementation). 3,4
Other U.S. consensus groups' recommendations remain more aggressive, standing by the recommendation that mammograms be initiated before age 50 with an annual screening interval (e.g., American Cancer Society, 5 American College of Obstetrics and Gynecology, 6 American College of Radiology 7 ). Despite this ongoing controversy, USPSTF recommendations are based on a rigorous review of randomized control trials and the research of the Cancer Intervention and Surveillance Modeling (CISNET) investigators 8 showing that for women aged 40–49 years who are at average risk for breast cancer, the benefits of screening mammography to reduce mortality are lower than for older women, whereas the risks of potential harms are higher (e.g., false-positive results, unnecessary biopsies, overdiagnosis). 3,4
Moreover, USPSTF guidelines align with those from other international professional societies. A recent comparison of breast cancer screening recommendations among 21 countries (most are European) showed that the most common age range for screening is generally from 50 to 69 years, and biennial screening is recommended in most of the selected countries. 9 Comparisons of the simulated aggregate cost of mammography screening in the United States showed that USPSTF recommendations (biennial between 50 and 74 years) would save $6.7 billion in 2010 compared with a policy of an annual mammography. 10
Relatively little research has assessed what factors influenced women's propensity to be screened in their 40s. 11 –13 In the context of not initiating mammography screening for average risk women in their 40s, women's screening plan could be impeded by: low awareness of the potential harms of mammography screening in this age range, 14 conflicts in mammography guidelines, 15 insurance coverage of mammogram starting at age 40 with little or no patient cost-sharing, 16 and previous communication campaigns that promote annual mammography beginning at age 40.
Together these social forces may lead to the inference that mammograms in one's 40s are appropriate medical care. 17 This along with documented misperceptions that breast cancer is more common than it is, and related worry and anxiety, 18 may inhibit receptivity to delaying mammography screening 19 or perceiving the need to consult a health care provider to consider delaying screening. Consideration of these factors will be important to any efforts to engage women at low risk for hereditary cancer to consider not initiating annual mammograms in their 40s.
To this end, we aimed to assess the extent to which women aged 40–49 years living in the United States who were deemed at low risk for hereditary breast cancer: (1) were aware of the USPSTF risk-stratified mammography screening guideline recommendations, (2) have ever engaged in mammography screening, and (3) were influenced in their decision about screening by their awareness of current recommendations and other individual-level factors.
Materials and Methods
Study design and population
We conducted an online population-based survey with a sample of U.S. women. The survey was administered by Ipsos KnowledgePanel®. Ipsos is a commercial survey company that uses probability-based sampling with address-based methods to randomly recruit households to the KnowledgePanel. 20 To increase the sample's representativeness to the U.S. population, households without internet access are provided with tablet computers and internet access. 21
In addition to sampling from the overall panel to create a cohort representative of U.S. women aged 40 through 49 years, the study team added two eligibility screening questions to identify women at low risk for hereditary breast and ovarian cancer. We asked women: “Is there any history of breast or ovarian cancer in your family? Think about both your mother and father's side of the family. Include yourself, parents, children, brothers/sisters, aunts/uncles, nieces/nephews, and grandparents.” Furthermore, we asked if their most recent screening was due to abnormal breast symptoms. Eligible individuals were: women, ages 40–49 years, English-speaking, without abnormal breast findings, and were identified at low risk for hereditary breast and ovarian cancer based on family history.
In October 2020, a random sample of 1645 U.S. women aged 40 through 49 years was drawn from Ipsos KnowledgePanel. Seven hundred twenty-nine (44.3%) women responded to the study invitation and completed the eligibility screener, and 383 (52.5%) were eligible and completed the online survey. All research activities were reviewed and approved by institutional review board at the Emory University.
Measures
Sociodemographic factors
Ipsos provided sociodemographic data about panel members, including age, race/ethnicity, education, income, employment and marital status, health insurance type, and access to primary care doctor.
Initiation of screening mammography
We asked women: “Have you ever had a mammogram?” We operationalized not having initiated screening to include women who responded “no” to this question. For women who responded “yes,” we asked them to report the age at which they had their first mammogram, and how frequently they have had mammograms in the past 2 years with categorical answers grouped to “annual or more” or “biennial or less.”
Awareness
Women were asked to indicate their familiarity (yes, no/unsure) with the following items. Awareness of the benefits and harms of mammography were assessed by three items adapted from a prior study. 22,23 Women were asked if they had heard about “Mammograms can provide peace of mind by finding that you do not have breast cancer” (benefit), “Mammograms can find something that looks like cancer but eventually turns out not to be cancer. This is called a ‘false-positive’ or ‘false alarm’” (harm), and “A ‘false-positive’ or ‘false alarm’ result will lead to tests that are unnecessary, painful, and expensive” (harm).
Awareness of the risk-stratified screening guideline was assessed by one-item: “National guidelines recommend that how often a woman has a mammogram should depend on her level of risk for breast cancer.” Awareness of guidelines regarding when to start mammograms and frequency. We provided women with the stem question, “Based on what you have heard about national recommendations for mammography screening for women like you,” and asked them to endorse recommended starting age and frequency. Responses were coded as “yes” if women responded “age 50” as the starting age and “once every two years” as the frequency, consistent with the current USPSTF guideline. 3,4
Belief in guideline screening recommendations. We asked women to what extent (not at all, somewhat, a great deal, don't know) they believed guideline recommendations on screening start age and frequency, with two items. Perceived risks. We used three 10-point Likert scale items (0 = not at all likely, 10 = extremely likely) to assess the following: likelihood of getting breast cancer before the age of 50, likelihood of avoiding dying from breast cancer if you have annual mammograms in your 40s, and likelihood of experiencing a “false-positive” or “false alarm” result if you have annual mammograms in your 40s.
Perceived importance of reducing chance of dying from breast cancer. In deciding when and how often to have mammogram screening, we asked women two questions to assess how important is it for them to reduce their chance of dying from breast cancer (benefit of mammograms) and to avoid false positives or false alarms of mammograms (harms of mammograms). Response options ranged from “not at all important” to “very important” on a 4-point Likert scale. We also assessed general cancer worry by asking participants 24,25 : “On a scale from 0 to 10, where 0 is not at all worried and 10 is extremely worried, how worried are you about getting breast cancer in your 40s?”
Data analyses
Once all survey data were collected and processed, design weights accounting for any differential nonresponse that may have occurred were calculated by Ipsos KnowledgePanel. The survey was weighted to be nationally representative of U.S. adult females aged 40 through 49 years. For this study, the following benchmark distributions from the most recent (March 2018) Current Population Survey data were used for the raking adjustment of weights: age, race/ethnicity, census region, metropolitan status, education, and household income.
We calculated frequencies and means to describe all variables. For bivariate analyses, the dichotomized outcome, have not initiated versus have initiated screening mammography, was regressed on each of the patient factors separately. We hypothesized that cancer worry would moderate the relationship between risk perceptions and the outcome and set out to test interaction terms if direct effects were statistically significant. The culminating analysis, a multivariable logistic regression model, includes theoretically and clinically relevant variables. Data analyses were performed using STATA Version 15.0 (STATA Corp, College Station, TX, USA).
Results
Characteristics of participants
A total of 383 women completed the survey. Their family history assessment indicated that they were at low risk for hereditary breast cancer, did not have abnormal breast findings, and thus were considered at average risk for breast cancer. The sample characteristics are presented in Table 1. Women were on average 45 years of age (standard error [SE] = 0.2), with 62% aged 40–45 years. More than half of women reported being White (53%). The majority of women were married (68%), employed (79%), and had a household annual income of more than $75,000 (60%). Most women were insured (98%) and reported having access to a primary care doctor when they have a health concern (82%).
Sample Characteristics Based on Weighted Survey Data
CI, confidence interval; SE, standard error; VA, Veterans Affairs.
Initiation of mammogram screening
The majority of women (71%) reported ever having been screened. Mammogram screening initiation age ranged from 16 to 49 years; 25% had the first mammogram before age 40, 32% started screening at age 40, and 14% started screening after age 40. More than half (61%) had screened at least once a year in the past 2 years. The reasons for their most recent mammogram were: a doctor's recommendation for routine screening (56%), personal choice (42%), or family/friend recommendation (1%).
Awareness of guideline
More than half of the women (57%) stated that they had heard about the risk-stratified screening guideline. However, women's awareness of the recommended age to initiate screening (age 50) and screening frequency (biennial) for those at low hereditary risk was low: 10% and 21%, respectively.
Awareness of benefit and harms of mammogram screening
Most women (70%) endorsed the notion that mammograms can provide peace of mind by finding that a person does not have breast cancer. Although awareness of the false-positive results of mammogram screening was high (81%), there was low awareness (43%) regarding the possibility of overdiagnosis or overtreatment.
Cancer-related risk perceptions, beliefs, and cancer worry
On average, women perceived their chance of getting breast cancer before age 50 to be very low (possible range: 0–10, mean = 2.6, 95% confidence interval [CI]: 2.3–2.9). Accordingly, breast cancer-related worry was also low (possible range: 0–10, mean = 3.5, SE = 0.2, 95% CI; 3.1–3.8). However, women believed that having annual mammograms in their 40s would reduce their chance of dying from breast cancer (possible range: 0–10, mean = 6.3, 95% CI: 5.9–6.7). Perceptions relating to harms of mammography, including a chance of getting a false-positive screen result from a mammogram in their 40s, appeared to be somewhat higher than concerns about their chance of getting breast cancer (possible range: 0–10, mean = 4.1, 95% CI: 3.8–4.4).
Just over one third of women reported a great deal of belief in guideline recommendations on screening start age (36%) and frequency (43%). In considering when to start and how often to have mammograms, women perceived the benefit of reducing the chance of dying from breast cancer to be of slightly greater importance (possible range: 1–4, mean = 3.6, 95% CI: 3.6–3.7) than their potential to experience harms related to false-positive screening results (possible range: 1–4, mean = 3.1, 95% CI: 2.9–3.2).
Factors associated with not initiating mammogram screening
Factors significantly associated with screening initiation identified in the bivariate logistic regressions were: age, access to a primary care doctor, awareness of screening initiation, age, perceived likelihood of false-positive results, and perceived importance of reducing chance of dying from breast cancer (Table 2).
Association Between Information Processing Factors and not Initiating Mammography Screening: Results from Bivariate and Multivariable Logistic Regressions with “Initiation of Screening Mammography” as the Reference Category
Perceived risk reduction potential of mammography was not included in the multivariable logistic regression model, as it appeared to be a mediator between awareness of guideline recommended screening age and initiation of mammogram screening. However, we could not formally test mediation as the study was not powered to do so.
OR, odds ratio.
Multivariable logistic regression analysis (Table 2) showed that women older than 45 years had lower odds of not having initiated mammography screening compared with women aged 40–45 years (odds ratio [OR] = 0.22, 95% CI: 0.10–0.47, p < 0.001). Women who were aware of the guideline recommendation to initiate screening at age 50 had higher odds of not initiating screening (OR = 6.70, 95% CI: 2.50–17.98, p < 0.001). However, women who had a primary care doctor had lower odds of not initiating screening (OR = 0.25, 95% CI: 0.12–0.54, p < 0.001). Other factors including race, awareness of false alarms, perceived importance of reducing chance of dying from breast cancer, cancer worry, and breast cancer risk perception did not make a statistically significant contribution to the model.
Due to nonsignificant direct effects of cancer worry and of all three variables assessing risk perceptions on mammography screening initiation in bivariate analyses (Table 2), we did not test for the moderation effect of cancer worry on the relationship between risk perceptions and women's screening behavior.
Discussion
Our findings are consistent with the contention that evidence-based guidelines that support risk-stratified screening established a decade ago have largely not been adopted by American women. 26 –29 The majority of women aged 40–49 years in this population-based sample reported having had at least one mammogram (71%) and many were having annual mammograms (61%). This proportion of screening is even higher than recent national statistics that show 60% use of mammography among women in their 40s. 26 Our sample included 25% of women who had their first mammogram before age 40, which is also higher than recent national estimates. Data from the 2011–2015 National Survey of Family Growth showed that among U.S. women aged 18–39 years with no personal cancer history, one in seven (14.3%) reported having received a mammogram. 30
Several national organizations consider that for average risk women aged 40–49 years, the potential harms of mammograms outweigh the benefits and thus screening is regarded to have “low value.” Indeed, mammography screening exposes women to unnecessary treatment, pain, side effects, and is expensive as it may divert limited screening resources from women in need. 10 Thus, ensuring that women gain a deeper understanding of appropriate mammography screening offers considerable potential benefits both to women and to health care systems.
Our results also showed that being aware of the updated screening start age (50 years) served as a facilitator to not initiating low-value screening. Women's awareness of risk-stratified mammography screening recommendations varies widely, based on the findings here. Given well-documented confusion about mammography recommendations reported in several studies, 15,17 more efforts are needed to promote guideline awareness as an initial step for thoughtful considerations of mammogram screening.
Contrary to our hypothesis, awareness of mammogram's benefits and harms was not associated with mammography screening among women in our study. Other studies have reported similar findings, with awareness of the harms of overdiagnosis and overtreatment not being associated with women's attitudes or intentions toward mammograms. 14,31 In our sample, women perceived the benefits for reducing risk of dying to be equally balanced with any concerns they had about the negative side effects of screening. Women in our sample also were largely unaware of the possibility of overtreatment.
Women's risk perceptions, perceived importance of benefits and harms, and cancer worry also were not significantly associated with women's screening behavior. Psychological theories such as the Dual Processing Model 32,33 lend insight into factors that could limit women's systematic or thoughtful processing of recommendations to delay mammograms. Indeed, systematic processing has consistently been shown to be associated with behavioral adoption. 34,35 This model suggests that women may be most likely to give thoughtful attention to recommendations not to initiate mammograms in the 40s when they perceive: mammography screening to be salient for health, the potential harms of mammography in one's 40s to outweigh the benefits of having a mammogram in one's 40s, and they have the capability to delay mammograms.
By contrast, less thoughtful or peripheral information processing is prompted by emotional reactions to the recommendation such as fear or worry. 35 Our findings suggest that women were not thoughtfully and critically processing the recommendation. Indeed, given that our sample generally perceived themselves to be at very low risk for breast cancer and were not particularly worried about dying from breast cancer, these women may be pursuing mammogram screening in the 40s almost automatically without much thoughtful consideration. Moreover, this automatic initiation may lead to an inertia noted by several studies that women continue annual screening and are less likely to forgo future mammograms. 25
Two factors reinforce this conclusion. Younger women were more likely not to have initiated mammograms than women older than 45 years, possibly due to that younger women may have not yet become habituated to the one-size-fits-all annual mammogram recommendations; and most of the benefit of screening women aged 40–49 years would be realized by starting screening at age 45. 3,4 Additionally, having access to a primary care provider was associated with a greater likelihood of having low-value mammography screening.
Multiple provider survey studies have shown physician recommendations for mammography screening to be in excess of those recommended by the USPSTF. 36 –38 Health systems and providers may resist not offering annual mammogram starting at age 40 due to medical malpractice concerns, 38 –40 and conflicting guideline recommendations. 15 Moreover, evaluation metrics for care quality and reimbursement policies focus less on overuse of practices versus underuse. 41 Future interventions could study multilevel determinants of overscreening and affect these areas in addition to the women's beliefs.
Taken together, these findings suggest the importance of developing de-implementation interventions that target both women and their health care providers. A recent systematic review and meta-analysis demonstrated that de-implementation interventions that engage patients through patient–provider interaction using patient education materials and shared decision-making tools have been successful in de-implementing low-value medications, surgeries, and diagnostic tests. 42 Given a provider's motivation to promote greater involvement of patients in mammogram screening decision-making, 43 engaging women and providers to initiate collaborative decision-making may hold the promise for successful de-implementation.
We acknowledge that mammogram screening is not a dichotomy, with the only options being to start annual screening at age 40 or to wait until age 50. As professional organizations disagree on recommendations, 9 it is important to acknowledge the impact of this conflicting information on women's screening behavior. The limitations of our study include the use of self-reported data. The survey had a 44% response rate. Although weighting helps to ensure that analyses reflect the demographic characteristics of U.S. adult females aged 40 through 49 years, this does not eliminate the possibility that those who chose to participate might be systematically different in their responses from those who did not.
In addition, our sample included women with relatively high education and income compared with the general population. Women in our study also reported relatively higher screening rates compared with national statistics for women at the same age range. It is possible that respondents to an online survey may differ from the general population. However, surveys of U.S. adults by Pew Research Center show that 93% of Americans now use the internet. 44 Furthermore, we did not assess other factors that may influence women's screening behavior (e.g., doctor–patient discussion about screening). For women who had prior mammogram screenings, we assessed only the reason for their most recent screening and the frequency of screening in the past 2 years.
Conclusions
This population-based survey study adds to the growing evidence base to uncover factors associated with women aged 40–49 years who engage in low-value mammography screening. A National Cancer Institute initiative calls for multilevel strategies to facilitate de-implementation of low-value clinical practices in cancer prevention and treatment. 45 Empirical research to reduce low-value cancer screening has been limited. 46 Future research is needed to examine multilevel strategies or interventions that are optimal for average risk populations in their decision-making about breast cancer screening plans.
Footnotes
Authors' Contributions
Study concept and design (Y.G., C.M.M., and C.E.), data analysis and interpretation of data (Y.G., R.H., C.M.M., J.L., and C.E.), preparation of article (Y.G.), and critical revision of article (R.H., C.M.M., J.L., and C.E.). All authors read and approved the final article.
Author Disclosure Statement
No competing financial interests exist.
Funding Information
Y.G. is funded by the Winship Cancer Institute of Emory University, through Winship Invest$ Winter 2020 Cycle.
