Chronic Medical Illness as a Risk Factor for Poor Mammography Screening Adherence

Abstract

Objective:

The aim of this study was to determine the association between the presence of chronic medical disease and mammography screening adherence.

Materials and Methods:

We performed a retrospective study on women between the ages of 50 and 64 who received screening mammography in 2005 and had at least 8 years of follow-up. Demographic and clinical information was obtained from our centralized patient data registry. Women diagnosed with one or more of the following diseases for at least 3 months before their index mammogram were considered to have a chronic disease, including atrial fibrillation, congestive heart failure, Chronic Obstructive Pulmonary Disease (COPD), diabetes mellitus type II, heart disease, and/or peripheral vascular disease. Generalized estimating equations were used to evaluate for correlated observations. Multivariable regression analyses were used to evaluate the effects of selected chronic medical diseases on longitudinal engagement with routine mammography.

Results:

Of 9575 women identified, 1669 (17.7%) had one or more of the selected chronic medical diseases. The presence of one or more of these diseases was associated with reduced mammography screening (−0.29; confidence interval [CI] = −0.36 to −0.14; p < 0.01) compared with women without these diseases over the study period. Within this group, the presence of congestive heart failure (−0.88; CI = −0.84 to −0.45; p ≤ 0.01), COPD (−0.39; CI = −0.57 to −0.21; p ≤ 0.01), or diabetes mellitus type II (−0.37; CI = −0.57 to −0.17; p ≤ 0.01) was individually associated with reduced screening compared with women without the respective disease. Compared with women without chronic medical disease, women with multiple chronic medical diseases (−0.62; CI = −0.93 to −0.30; p ≤ 0.01) were significantly (p ≤ 0.05) less likely to receive routine screening, while no significant difference was seen in women with only one chronic medical disease (−0.18; CI = −0.39 to −0.02; p ≤ 0.08).

Conclusion:

Despite experiencing longer life expectancies, women with specific chronic diseases may experience additional barriers to uptake of mammography screening, which is likely compounded by the comorbidity burden of being simultaneously treated for multiple chronic conditions. Increased health care interactions seen in this group may represent missed opportunities to improve screening adherence.

Introduction

There is robust evidence supporting the population-based benefits of routine screening mammography.^1
–3 The United States Preventative Services Task Force (USPSTF) currently recommends biennial screening mammography for average-risk women aged 50–74 years.⁴ The effectiveness of mammography screening, however, depends on the maintenance of routine examinations among eligible women, which has been estimated to reduce breast cancer mortality by up to 30%.⁵ As a result, efforts to identify and address barriers to routine mammography screening have become important public health issues. Previously described factors contributing to reduced screening rates in US women include race/ethnicity, income, education, health care access, lifestyle, geographic location, and English proficiency.^{6

–15}

The influence of chronic diseases on routine screening mammography adherence, however, remains controversial. While some studies have shown no association between the presence of chronic medical disease and routine mammography screening, others have demonstrated decreased screening rates in this population despite increased health care interactions compared with women without these conditions.^{16

–23} Proposed reasons contributing to possible decreased screening in this population include prioritization of chronic disease management over health maintenance examinations and expected shortened life expectancy.¹⁶ In contrast, a few studies have demonstrated increased screening mammography utilization in these women compared with women without chronic medical disease.^24

–27

The prevalence of chronic disease has increased significantly over the past couple of decades, representing nearly 50% of the US health burden.²⁸ This has largely been influenced by advances in chronic disease management, which has led to increased lifespans among women living with chronic medical conditions. Both increased breast cancer risk and all-cause mortality are seen in this population compared with women without chronic medical diseases, supporting the importance of early detection in this growing population.^29

–34

Breast cancer screening is recommended in women of screening-eligible age with life expectancy of at least 5–10 years.^35,36 Increasing numbers of women with chronic medical diseases who now demonstrate increased life expectancies in the United States may, therefore, benefit from routine mammography screening. While prior studies have not restricted their analyses to women with long-term follow-up after starting routine screening, our goal was to evaluate the influence of chronic medical diseases on screening mammography in a cohort of women with long-term (≥8 years) medical follow-up, who, based on recommendations, should be receiving routine mammography.^18,19

Materials and Methods

Study setting and population

We performed a retrospective, longitudinal cohort study of women between the ages of 50 and 64 within a large health care network in Boston, MA, who received a screening mammogram in our hospital system during the calendar year of 2005. Women were followed from the time of their index examination in 2005 until December 2015. Women with <8 years of clinical follow-up during the study period were excluded. Patient records were searched using our Research Patient Data Registry (RPDR) system, a centralized clinical data registry that allows clinical information including sociodemographic, medical diagnosis, imaging, and management/treatment data to be queried from patient records in our affiliated network hospital and health care systems without the need for coded information.¹⁸

Data collection

The RPDR tool was used to identify women meeting inclusion criteria, who received a screening mammogram in our hospital system during the calendar year of 2005. Sociodemographic information was collected from these women, including age at baseline mammogram, race, primary language, marital status, and insurance status. Women with common chronic diseases, including atrial fibrillation, congestive heart failure, Chronic Obstructive Pulmonary Disease (COPD), diabetes mellitus type II, heart disease, and peripheral vascular disease, were identified. Medical diseases selected were based on commonly used ICD-9 codes in our system and prior studies.^16,19,23,27

Exposures

Primary exposure included a chronic disease diagnosis, defined as a claim for medical disease (atrial fibrillation, congestive heart failure, COPD, diabetes mellitus type II, heart disease, and peripheral vascular disease) diagnosis documented in the chart for at least 3 months before index mammogram in 2005 in the patient's chart. The ICD-9 codes used for each chronic medical disease included atrial fibrillation (427.3, 427.31), congestive heart failure (398.91, 402.11, 402.91, 404.91, 428, 428.0, 428.1, 428.2, 428.20, 428.21, 428.22, 428.23, 428.30, 428.31, 428.32, 428.33, and 428.9), COPD (496), diabetes mellitus type II (250.40, 250.42, 250.50, 250.52, 250.60, 250.62, 250.70, 250.72, 250.80, 250.82, 250.90, 250.92), heart disease (398.9, 398.90, 398.99, 402, 411.89, 414, 414.8, 414.9, 416.8, 416.9, 429.82, 429.89, 429.9), and peripheral vascular disease (443, 443.8, 443.89, 443.9). A summary index variable (yes/no) was constructed to evaluate if women had at least one of the previously listed chronic disease diagnoses before their index mammogram in 2005. Women with “any chronic disease” were considered to have one or more of any of the previously described diseases.

Outcomes

Primary outcome was adherence to recommended routine mammography guidelines measured every 2 years for the 10-year study period. Screening mammography engagement was defined as adherence with recommended routine mammography guidelines (yes/no) at each 2-year interval following the index screening mammogram in 2005 until December 2015 (longitudinal binary response outcome). Having at least one mammogram (screening or diagnostic) during the subsequent 2-year intervals (10-year total follow-up time) following the index mammogram was considered adherence for that particular period based on guidelines from the USPSTF. Either screening or diagnostic mammograms were considered adherence after the index mammogram since (1) the clinical protocol at our hospital system requires women receiving a diagnostic examination, who are due for routine screening, to undergo bilateral screening in addition to their diagnostic work-up and (2) only one mammogram was required to represent adherence over a 2-year interval.

Potential confounders and effect modifiers

Baseline sociodemographic variables including age, race category (White, Black, Hispanic, Asian, other), marital status (married, single, divorced, widow, other), insurance category (commercial, Medicare, Medicaid, other), and English as primary language (yes/no) were considered potential confounders.

Statistical analysis

Baseline demographic characteristics were described for our study cohort using means and proportions. Descriptive analyses were performed to quantify screening mammography outcomes, including total number of screening mammograms.

For our primary analysis evaluating routine mammography engagement at multiple time points, we used generalized estimating equations to evaluate for correlated binary response outcomes. Unadjusted (bivariate) regression analyses were conducted evaluating the effects of each chronic disease on longitudinal engagement with screening mammography. Multiple variable regression analyses were conducted evaluating the effects of chronic disease on longitudinal engagement with screening mammography, adjusting for potential confounders (age, race category, insurance status, primary language, marital status). Additional multiple variable regression analyses were then conducted evaluating the association between having either one or multiple (≥1) chronic diseases compared with women without chronic medical disease. Regression coefficients with 95% confidence intervals (CIs) were presented with two-tailed p-values <0.05 considered statistically significant. Analyses were conducted using STATA 11(StataCorp, College Station, TX).

Results

A total of 9575 women met inclusion criteria. Sociodemographic characteristics of these women are presented in Table 1. Most women were white (8092/9575; 84.5%), primary English speakers (8958/9575; 93.6%), and married (5389/9575; 56.3%). The majority of women also had commercial (4614/9575; 48.2%) or Medicare (4738/9575; 49.5%) insurance.

Table 1.

Sociodemographic Data

Patient characteristics	N	%
Age (years)
50–54	3588	37.5
55–59	3457	36.1
60–64	2530	26.4
Race
White	8092	84.5
Black	456	4.8
Hispanic	291	3.0
Asian	355	3.7
Other	381	4.0
Primary language
English	8958	93.6
Other	617	6.4
Marital status
Married	5389	56.3
Single	2209	23.1
Divorced	865	9.0
Widow	643	6.7
Other	469	4.9
Insurance status
Private	4614	48.2
Medicare	4738	49.5
Medicaid	152	1.6
Other	71	0.7

A total of 1669 (17.4%) women had one or more of the selected chronic medical diseases. Heart disease (625/9575; 6.5%) was the most common chronic medical disease, followed by COPD (455/9575; 4.8%), diabetes mellitus type II (403/9575; 4.2%), congestive heart failure (263/9575; 2.8%), peripheral vascular disease (262/9575; 2.7%), and atrial fibrillation (183/9575; 1.9%).

The rate of adherence to screening mammography guidelines during the 10-year study period was 72.4% among women without a chronic medical disease, as compared with 66.3% among women with at least one chronic medical disease. This trend was seen in each disease category comparing women without disease versus women with disease: atrial fibrillation (71.5% vs. 64.5%), congestive heart failure (71.8% vs. 54.0%), COPD (71.8% vs. 62.2%), diabetes mellitus type II (71.7% vs. 62.8%), heart disease (71.5% vs. 69.8%), and/or peripheral vascular disease (71.8% vs. 64.1%) (Table 2).

Table 2.

Screening Mammography Engagement

	Total patients with			Total patients without
Chronic disease	N	%	Screening mammography engagement (%)	N	%	Screening mammography engagement (%)
Atrial fibrillation	183	1.9	64.5	9392	98.1	71.5
Congestive heart failure	263	2.7	54.0	9312	97.3	71.8
COPD	455	4.8	62.2	9120	95.2	71.8
Diabetes mellitus type II	403	4.2	62.8	9172	95.8	71.7
Heart disease	625	6.5	69.8	8950	93.5	71.5
Peripheral vascular disease	262	2.7	64.1	9313	97.3	71.5
Any chronic disease (one or more)	1669	17.4	66.3	7906	82.6	72.4

COPD, Chronic Obstructive Pulmonary Disease.

There was a significant (p < 0.05) association between women with chronic medical disease (any chronic medical disease) and reduced mammography screening rates (−0.29; CI = −0.36 to −0.14; p < 0.01) compared with women without chronic medical disease after multiple variable analysis. Reduced screening was seen in each chronic medical disease group compared with women without the corresponding disease. The association between chronic medical disease and reduced screening mammography was only statistically significant, however, in women with congestive heart failure (−0.88; CI = −0.84 to −0.45; p ≤ 0.01), COPD (−0.39; CI = −0.57 to −0.21; p ≤ 0.01), and diabetes mellitus type II (−0.37; CI = −0.57 to −0.17; p ≤ 0.01) (Table 3).

Table 3.

Multiple Variable Regression Analysis of the Association Between Chronic Medical Disease and Screening Mammography Engagement

Chronic disease	Coefficient	Confidence interval	p-Value
Atrial fibrillation	−0.23	−0.52 to 0.06	0.12
Congestive heart failure	−0.88	−0.84 to −0.45	<0.01
COPD	−0.39	−0.57 to −0.21	<0.01
Diabetes mellitus II	−0.37	−0.57 to −0.17	<0.01
Heart disease	−0.11	−0.28 to 0.06	0.21
Peripheral vascular disease	−0.21	−0.46 to 0.04	0.11
Any chronic disease (one or more)	−0.29	−0.36 to −0.14	<0.01

Bold values represent statistically significant values (p < 0.05).

Women with multiple chronic medical diseases (−0.62; CI = −0.93 to −0.30; p ≤ 0.01) were significantly (p < 0.05) less likely than women without chronic medical disease to receive screening, while no significant difference was seen in women with only one chronic medical disease (−0.18; CI = −0.39 to −0.02; p = 0.08). (Table 4)

Table 4.

Multiple Variable Regression Analysis of Cumulative Chronic Medical Disease Burden and Screening Mammography Engagement

Presence of chronic disease	Coefficient	Confidence interval	p-Value
None	1	—	—
One chronic disease	−0.18	−0.39 to −0.02	0.08
Multiple (>1) chronic diseases	−0.62	−0.93 to −0.30	<0.01

Bold values represent statistically significant values (p < 0.05).

Discussion

In our retrospective analysis of women undergoing screening mammography who received medical follow-up for up to 10 years, nearly 18% had at least one of the selected chronic medical diseases included in our study. Under current screening guidelines, many of these women should be receiving routine screening mammography considering their extended life expectancy.³⁵ Despite demonstrating longitudinal follow-up of this population, reduced mammography screening rates were seen in patients with chronic medical disease compared with women without these conditions. Within this group, the presence of congestive heart failure, COPD, or diabetes mellitus type II was individually associated with reduced mammography screening compared with women without the respective disease. These differences, however, may be largely driven by the comorbidity burden of simultaneously being treated for multiple chronic diseases.

Women with chronic medical conditions have been shown to visit their health care providers at increased rates compared with women without these conditions.^16,19 It is unclear, however, whether increased medical engagement for chronic disease management facilitates or hinders discussions about cancer prevention. While increased patient–provider communication may offer increased opportunities to discuss preventative health maintenance examinations, specialized care for chronic conditions may cause issues such as routine maintenance examinations to be overlooked due to health management prioritization and time limitations.

Our study is consistent with prior studies demonstrating reduced screening rates in women with chronic medical disease.^16,37,38 Liu et al. have found that women with chronic lung disease and cardiovascular disease treated at four primary care clinics located in two rural communities in Oregon were less likely to be up-to-date with mammography screening than women without these conditions.¹⁶ The influence of chronic conditions on screening rates was shown to be disease-specific, however, as women with chronic digestive disorders were more likely to receive routine screening. Constantinou et al. have demonstrated similar findings in women with diabetes, similar to our study population, but not with other chronic conditions.³⁷ Their group proposed that chronic conditions requiring active management during medical visits may require more attention at the expense of discussions about preventative practices such as cancer screening. This increased emphasis on specialized care likely played a role in our study. Chronic cardiovascular and lung diseases are likely to be associated with other comorbid chronic diseases contributing to increased specialist care rather than primary care, influencing utilization of routine preventative services. This is supported in our study, as women with multiple comorbid chronic diseases (≥1 chronic disease) were less likely to receive screening compared with women without chronic medical disease, while no significant difference was seen in women with only one chronic medical disease. Furthermore, Kiefe et al. have shown that each unit of increase in the comorbidity index in women with chronic medical disease corresponded with a 17% decrease in the likelihood of mammography screening, potentially supporting the negative influence of added medical management on maintenance examinations in women with chronic medical diseases.³⁸

Our findings are in contrast to those of Guo et al., who did not show an association between chronic medical disease and decreased mammography screening.²⁷ Their group evaluated women with hypertension, previous myocardial infarction, stroke, coronary heart disease, and other heart problems. Screening mammography rates in their study may have been overestimated due to recall and social response bias, however, since screening mammography use was self-reported. Similarly, many other studies demonstrating no association between presence of chronic medical disease and routine screening have used survey data and presented similar limitations.

Increased medical visits experienced by women with chronic medical diseases may represent missed opportunities for the use of mammography screening services.^39
–41 Lack of physician recommendation has been shown to represent a potential barrier to mammography screening, which may influence decreased screening in these women.⁴² Targeted messaging to physicians who treat these women, especially those providing subspecialty care, about addressing preventative health maintenance examinations may be necessary to increase awareness of this issue. In this population, both benefits and harms of screening should be discussed considering the severity of disease, life expectancy, and patient preferences.³⁴ While not all women meeting screening guidelines with chronic medical disease should be screened with routine mammography based on these factors, conversations on this topic should not be avoided given the increased prevalence of chronic medical diseases in the United States and advances in medical management leading to longer life expectancy among this population. Due to potential time limitations associated with clinical visits for these women, interventions that limit the burden on direct patient–provider interactions should also be considered, including ancillary staff-initiated correspondence reminding women about staying up-to-date with routine screening examinations. Overall, increased education and advocacy regarding this topic among legislators, providers, and women will be required to address this emergent issue.

Our study has numerous strengths, including assessment of the association of multiple chronic medical conditions with routine mammography screening. Disease management varies significantly among different chronic conditions, which likely affects how specific conditions influence mammography screening rates. We also obtained data through medical chart abstraction rather than self-report, limiting recall and social response bias. Additionally, while many studies previously evaluating this association have used a combined comorbidity index, we were able to evaluate women with individual chronic medical conditions comparing them directly with women without the respective condition. Lastly, we utilized USPSTF breast screening guidelines for our analyses, which are the most conservative mammography screening recommendations to assess screening adherence to account for variation in practice.

Our study also has limitations. It was restricted to a limited number of hospitals within a large health care network in the northeastern United States and demonstrates limited racial diversity. Our study, however, was performed in a large metropolitan setting, increasing generalizability of our study. Additionally, we were unable to collect information regarding primary versus specialty care visits, quality of life, and functional status of women with chronic medical disease in our study, which may inform screening recommendations. Future studies should consider these factors.

In conclusion, women with specific chronic diseases may experience barriers to the uptake of routine mammography screening, despite now having longer life expectancies. Increased health care interactions seen in this group may represent missed opportunities of screening mammography adherence. Educational tools intended to educate and inform providers treating these women about the increasing importance of routine screening may be needed to improve mammography screening adherence in appropriate women with chronic medical diseases. Specifically, radiologists can play a greater role in increasing awareness on this issue by providing educational information online, including on social media platforms, presenting the importance of screening adherence in appropriate patients at medical specialty conferences, and engaging with patients with chronic diseases when they are seen in the mammography suite. Future studies should focus on understanding specific barriers faced by women with individual chronic medical diseases.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

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