Optimal breast cancer screening strategies for older women: current perspectives

Figures & data

Table 1 Guideline recommendations about screening mammography in older women

USPSTF guidelines	ACS guidelines	ACR guidelines	AGS guidelines
Offer biennial screening to women aged 50–74 years. Evidence is insufficient to recommend for or against screening in women >74 years of age. “I” statement*. The Task Force encourages more research on the topic.	Offer screening to women aged ≥45 years and continue as long as a woman is in good health and has life expectancy of ≥10 years.	Offer annual screening to women aged ≥40 years and continue as long as a woman is in good health.	Offer screening to women aged ≤85 years who have life expectancy of ≥5 years and for healthy women aged ≥85 years who have excellent functional status or who feel strongly about the benefits of screening (no screening frequency specified).

Notes:

* Current evidence is insufficient to address benefits and harms of breast cancer screening in women >74 years of age.

Abbreviations: ACR, American College of Radiology; ACS, American Cancer Society; AGS, American Geriatrics Society; USPSTF, US Preventive Services Task Force.

Table 2 Summary of studies assessing comorbidity, cognitive/functional status, and general health effects on mammography utilization in older women

Source (sample size)	Study design	Assessment of comorbidity/functional status	Assessment of mammography utilization	Key findings
				Comorbidity	Functional status
Mayer et al^Citation41 (N=995)	Randomized control trial	Questionnaire	Questionnaire: ≥1 screen within 2 years		Perceived general health: Good vs poor/fair OR =0.82 (95% CI: 0.50–1.30) Very good vs poor/fair OR =1.10 (95% CI: 0.70–1.90) Excellent vs poor/fair OR =0.87 (95% CI: 0.50–1.50)
Ives et al^Citation38 (N=2,205)	Prospective cohort study	Outpatient medical record, medicare insurance claims	Medicare insurance claims: ≥1 screen within 2 years	MMSE: MMSE: ≤23 vs ≥24 OR =0.98 (95% CI: 0.62–1.57) Depression: CES-D <16 vs ≥16 OR =0.76 (95% CI: 0.56–1.04)	ADL limitations: Yes vs no OR =0.56 (95% CI: 0.34–0.93) IADL limitations: Yes vs no OR =0.92 (95% CI: 0.75–1.14)
Blustein andWeiss^Citation37 (N=2,352)	Retrospective cohort study	Interview	Medicare claims: ≥1 screen within 2 years	Alzheimer’s/mental disorder: OR =0.55 (95% CI: 0.35–0.87)	ADL limitations: Yes vs no OR =0.71 (95% CI: 0.59–0.85) Perceived general health: Poor vs excellent OR =0.41 (95% CI: 0.26–0.56) Fair vs excellent OR =0.81 (95% CI: 0.58–1.13) Good vs excellent OR =0.84 (95% CI: 0.60–1.18) Very good vs excellent OR =1.15 (95% CI: 0.85–1.56)
Kiefe et al^Citation28 (N=1,764)	Cross-sectional study on retrospective defined cohort study	Medical records review	Medical records review: ≥1 screen within 2 years	Charlson comorbidity (1 unit increase): OR =0.83 (95% CI: 0.72–0.94)
Wright et al^Citation29 (N=683)	Cross-sectional population-based study	Telephone interview and medical records	Chart review/medical records: ≥1 screen within 2 years	Charlson comorbidity (1 unit increase): OR =0.90 (95% CI: 0.74–1.09)	ADL/IADL limitations (1 unit increase): OR =0.70 (95% CI: 0.53–0.94) Perceived general health (1 unit increase): OR =1.19 (95% CI: 0.99–1.42)
Caplan^Citation22	Prospective cohort study	Interview	Interview		ADL limitations: (Yes vs no) 36.0% vs 52.7% (P-value <0.001)
Scinto et al^Citation39 (N=844)	Prospective cohort study	Interview and self-report	Medicare claims: ≥1 screen within 5 years		ADL limitations: (Yes vs no) 12.5% vs 35.6% (P-value =0.001) Life expectancy (5-year mammography proportion): Grade 1 (best) – 47.5% Grade 2 – 27.3% Grade 3 – 18.2% Grade 4 (worst) – 7.0% (P-value =0.0001)
Wu et al^Citation35 (N=1,403)	Prospective cohort study	Interview	Interview	Number of conditions: ≥2 vs 0–1 OR =0.70 (95% CI: 0.54–0.90) MMSE: MMSE: ≤23 vs ≥24 OR =0.83 (95% CI: 0.63–1.09)
Heflin et al^Citation32 (N=1,481)	Cross-sectional within prospective cohort study	Interview	Self-reported: ≥1 screen within 2 years	Number of conditions: ≥3 vs 0–2 OR =1.35 (95% CI: 1.06–1.71) Cognitive impairment (1 unit increase): OR =0.95 (95% CI: 0.66–1.35) Depression: CES-D <9 vs ≥9 OR =1.22 (95% CI: 0.82–1.81)	IADL limitations (1 unit increase): OR =0.94 (95% CI: 0.87–1.03)
Schootman and Jeffe^Citation40 (N=10,639)	Cross-sectional population-based study	Questionnaire	Self-reported		ADL limitations: Short-term vs none OR =0.74 (95% CI: 0.36–1.51) Long-term vs none OR =0.18 (95% CI: 0.07–0.44) IADL limitations: Short-term vs none OR =0.86 (95% CI: 0.51–1.46) Long-term vs none OR =0.40 (95% CI: 0.22–0.73)
Schonberg et al^Citation34 (N=882)	Cross-sectional population-based study	Self-reported/questionnaire	Self-reported: ≥1 screen within 2 years	Number of conditions: 1 vs 0 OR =0.84 (95% CI: 0.57–1.22) ≥2 vs 0 OR =0.63 (95% CI: 0.38–1.06)	ADL/IADL limitations: IADL dep vs none OR =0.65 (95% CI: 0.40–1.05) ≥1 ADL vs none OR =0.44 (95% CI: 0.22–0.88)
Walter et al^Citation44 (N=3,988)	Cross-sectional population-based study	Self-reported	Self-reported: ≥1 screen within 2 years		Perceived general health: 1 (best) vs 4 (worst) OR =0.80 (95% CI: 0.60–1.00) 2 vs 4 OR =1.20 (95% CI: 0.90–1.60) 3 vs 4 OR =1.10 (95% CI: 0.90–1.50)
Bynum et al^Citation46 (N=722,310)	Retrospective cohort study	Medicare claims	Medicare claims: ≥1 screen within 2 years		Life expectancy (proportion receiving mammography): Grade 1 (low propensity to die) – 61% Grade 2 – 49% Grade 3 – 33% Grade 4 – 19% Grade 5 (high propensity to die) – 5% (P<0.001)
Thorpe et al^Citation49 (N=3,655)	Cross-sectional population-based study	Mental component survey	Self-reported: ≥1 screen within 2 years	Psychological distress: High level vs none OR =0.68 (95% CI: 0.34–1.37)
McBean and Yu^Citation30 (N=16,394)	Cross-sectional population-based study	Medicare claims	Medicare claims: ≥1 screen within 2 years	Charlson comorbidity: 1 vs 0 OR =0.87 (95% CI: 0.76–0.99) ≥2 vs 0 OR =0.65 (95% CI: 0.58–0.72)
Schonberg et al^Citation42 (N=4,683)	Cross-sectional population-based study	Self-reported	Self-reported: ≥1 screen within 2 years		Perceived general health: Avg vs above avg OR =0.74 (95% CI: 0.57–0.96) Below avg vs above avg OR =0.51 (95% CI: 0.37–0.70)
Williams et al^Citation47 (N=4,222)	Cohort study	Outpatient medical record	Self-reported: ≥1 screen within 2 years		Life expectancy Good prognosis: Middle income vs low income RR =1.08 (95% CI: 0.96–1.21) High income vs low income RR =1.18 (95% CI: 1.05–1.32) Limited prognosis: Middle income vs low income RR =1.18 (95% CI: 0.77–1.81) High income vs low income RR =1.92 (95% CI: 1.20–3.09)
Mehta et al^Citation48 (N=2,131)	Cross-sectional population-based study	Outpatient medical record	Medicare claims: ≥1 screen within 2 years	Cognitive impairment: Mild vs none OR =0.82 (95% CI: 0.60–1.10) Severe vs none OR =0.46 (95% CI: 0.30–0.80)
Reyes-Ortiz and Markides^Citation36 (N=1,272)	Prospective cohort study	Interview	Interview: ≥1 screen within 2 years	MMSE MMSE: ≤18 vs >18 OR =0.62 (95% CI: 0.45–0.86) Depression: CES-D: <16 vs ≥16 OR =1.42 (95% CI: 1.04–1.94)	IADL limitations: ≥4 vs 0–3 OR =0.65 (95% CI: 0.49–0.86)
Caban et al^Citation33 (N=4,610)	Prospective cohort study	Interview	Self-reported	Number of conditions: 1 vs 0 OR =1.14 (95% CI: 0.97–1.34) 2 vs 0 OR =1.21 (95% CI: 0.98–1.49) ≥3 vs 0 OR =1.56 (95% CI: 1.13–2.10) Cognitive impairment: Yes vs no OR =0.93 (95% CI: 0.75–1.15) Depression (last 12 months): Yes vs no OR =0.99 (95% CI: 0.75–1.34)	ADL/IADL limitations: Moderate vs none OR =0.98 (95% CI: 0.81–1.18) Severe vs none OR =0.67 (95% CI: 0.54–0.83) Perceived general health: Fair/poor vs excellent/very good/good OR =0.80 (95% CI: 0.66–0.96)
Tan et al^Citation31(N=697,825)	Retrospective cohort study	Outpatient medical record	Medicare claims: ≥1 screen within 2 years	Charlson comorbidity (proportion ranges): Charlson score =0 (13.3%–55.3%) Charlson score =1 (12.6%–55.9%) Charlson score =2 (8.3%–49.9%) Charlson score ≥3 (6.8%–37.9%)
Schonberg et al^Citation45 (N=2,266)	Cross-sectional population-based study	Self-reported	Self-reported: ≥1 screen within 2 years		Life expectancy: Medium vs low OR =1.40 (95% CI: 1.00–1.90) High vs low OR =2.40 (95% CI: 1.60–3.70)
Koya et al^Citation43 (N=4,836)	Cross-sectional population-based study	Self-reported/questionnaire	Self-reported: ≥1 screen within 1 year		Perceived general health: Excellent/very good vs fair/poor OR =1.12 (95% CI: 0.85–1.49) Good vs fair/poor OR =1.18 (95% CI: 0.90–1.54) Life expectancy: Intermediate risk vs low risk OR =0.69 (95% CI: 0.53–0.90) High risk vs low risk OR =0.37 (95% CI: 0.27–0.49) Very high risk vs low risk OR =0.22 (95% CI: 0.13–0.36)

Abbreviations: ADL, activities of daily living; avg, average; CES-D, Center for Epidemiological Studies-Depression; CI, confidence interval; IADL, instrumental activities of daily living; MMSE, mini-mental state examination; OR, odds ratio; RR, relative risk.

Table 3 Summary of findings from studies that evaluated the benefits, harms and the balance of benefits versus harms of screening mammography in older women

Source	Subgroups (years)	Outcomes reported
Benefits
McPherson et al^Citation63		RR of death and 95% CI
Screening groups: Mammographic vs clinical (palpation) diagnosis	Comorbidity	No comorbidity		Moderate	Severe
	Ages: 65–69	0.44 (0.32–0.59)		0.32 (0.15–0.69)	0.41 (0.11–1.48)
	Ages: 70–74	0.32 (0.23–0.44)		0.45 (0.22–0.91)	0.30 (0.11–0.79)
	Ages: 75–79	0.36 (0.26–0.49)		0.47 (0.25–0.88)	0.53 (0.20–1.36)
	Ages: ≥80	0.66 (0.52–0.83)		0.52 (0.33–0.80)	0.64 (0.30–1.87)
Fleming et al^Citation62		OR (and P-value) of late-stage (regional and distant) vs early stage (in situ and local) disease, under comorbid conditions
Screening groups: All patients were screened	Comorbidity OR (P-value)	Cardiovascular disease		Pulmonary disease, mild/moderate	Gastrointestinal disease, severe
		0.87 (P<0.01)		1.08 (P>0.05)	0.94 (P>0.05)
		Diabetes		Genital-urinary disease	Rheumatologic disease
		1.19 (P<0.01)		0.91 (P>0.05)	1.02 (P>0.05)
		Musculoskeletal disease		Renal disease	Other vascular disease
		0.93 (P<0.01)		1.15 (P>0.05)	1.04 (P>0.05)
		Benign breast disease, nonmalignant		Osteoporosis	Psychiatric disease
		0.76 (P<0.01)		1.16 (P>0.05)	1.2 (P<0.01)
		Cerebrovascular disease		Malignant hypertension	Gastrointestinal disease
		1.03 (P>0.05)		1.02 (P>0.05)	0.86 (P<0.01)
		Osteoarthritis		Neurological disease	AIDS
		0.96 (P>0.05)		1 (P>0.05)	1.41 (P>0.05)
		Benign hypertension		Pulmonary disease, severe	Hematologic disease
		0.98 (P>0.05)		0.99 (P>0.05)	1.19 (P<0.01)
		Endocrine disease		Obesity	Other cancers
		1.11 (P<0.05)		1.18 (P>0.05)	1.04 (P>0.05)
Braithwaite et al^Citation61		OR and 95% CI for invasive breast cancer vs DCIS
Screening groups: 2- vs 1-year interval		2- vs 1-year interval
	Comorbidity	Charlson score =0		Charlson score ≥1
	Ages: 66–74	0.83 (0.59–1.17)		0.92 (0.54–1.56)
	Ages: 75–89	1.07 (0.71–1.60)		1.02 (0.51–2.03)
		OR and 95% CI for advanced stage (stages IIB–IV) vs early stage (stages I–IIA)
	Comorbidity	Charlson score =0		Charlson score ≥1
	Ages: 66–74	0.75 (0.46–1.22)		0.99 (0.48–2.04)
	Ages: 75–89	1.27 (0.72–2.25)		0.37 (0.13–1.04)
		OR and 95% CI for large size tumors (>20 mm) vs small (≤20 mm)
	Comorbidity	Charlson score =0		Charlson score ≥1
	Ages: 66–74	0.83 (0.55–1.24)		0.91 (0.50–1.65)
	Ages: 75–89	1.30 (0.83–2.05)		1.38 (0.70–2.73)
		OR and 95% CI for positive lymph node involvement
	Comorbidity	Charlson score =0		Charlson score ≥1
	Ages: 66–74	0.84 (0.57–1.23)		0.76 (0.41–1.43)
	Ages:75–89	0.83 (0.51–1.33)		0.62 (0.29–1.34)
Mandelblatt et al^Citation64		Long-term quality-adjusted marginal savings in life-expectancy (in days) and 95% CI
Screening groups: Screening vs no screening	Comorbidity	Average health	Mild hypertension	Congestive heart failure	Average health (black)
	Ages: 65–69	2.19 (1.97, 2.41)	1.97 (1.77, 2.16)	1.17 (1.06, 1.28)	2.17 (1.95, 2.39)
	Ages: 70–74	1.85 (1.67, 2.03)	1.68 (1.51, 1.84)	1.08 (0.98, 1.18)	2.22 (1.99, 2.44)
	Ages: 75–79	1.43 (1.30, 1.57)	1.32 (1.20, 1.44)	0.91 (0.83, 0.98)	1.76 (1.59, 1.94)
	Ages: 80–84	1.08 (0.98, 1.18)	1.01 (0.92, 1.10)	0.76 (0.69, 0.82)	1.65 (1.49, 1.80)
	Ages: ≥85	0.80 (0.73, 0.87)	0.76 (0.69, 0.83)	0.59 (0.54, 0.65)	1.16 (1.05, 1.27)
		Long- and short-term quality-adjusted marginal savings in life-expectancy (in days) and 95% CI
	Comorbidity	Average health	Mild hypertension	Congestive heart failure	Average health (black)
	Ages: 65–69	1.44 (1.22, 1.66)	1.22 (1.03, 1.42)	0.43 (0.31, 0.54)	1.42 (1.20, 1.64)
	Ages: 70–74	1.10 (0.92, 1.28)	0.93 (0.77, 1.09)	0.33 (0.23, 0.44)	1.47 (1.25, 1.69)
	Ages: 75–79	0.69 (0.55, 0.82)	0.57 (0.45, 0.70)	0.16 (0.08, 0.24)	1.01 (0.84, 1.19)
	Ages: 80–84	0.34 (0.24, 0.44)	0.27 (0.17, 0.36)	0.01 (−0.06, 0.07)	0.90 (0.74, 1.06)
	Ages: ≥85	0.05 (−0.02, 0.12)	0.01 (−0.06, 0.08)	−0.15 (−0.20, −0.10)	0.42 (0.31, 0.56)
Messecar^Citation66		Quality-adjusted savings in life-expectancy, quality-adjusted life-years (in days)
Screening groups: One additional screening following biennial screening vs no prior screening	Subgroups	Following regular biennial screening		No prior screening
	Comorbidity	Cognitive impairment	Healthy	Cognitive impairment	Healthy
	Ages: 75–79	0.004 (1.5)	0.009 (3.3)	0.055 (20)	0.119 (43.4)
	Ages: 80–84	0.002 (0.7)	0.007 (2.5)	0.025 (9.1)	0.089 (32.5)
	Ages: ≥85	0.001 (0.4)	0.006 (2.2)	0.015 (5.5)	0.071 (25.9)
Lansdorp-Vogelaar et al^Citation65	Incremental LYG per 1,000 individuals screened according to guidelines since 50 years of age in populations with average comorbidity, by model, and age of screening cessation
Screening groups:Age of screening cessation	Comorbidity	Average comorbidity
	Model	MISCAN-Fadiaa	SPECTRUM^b
	Age of cessation =74 (vs 72)	7.6	5.8
	Age of cessation =76 (vs 74)	6.9	5.1
	Deaths prevented per 1,000 individuals screened according to guidelines since 50 years of age in populations with average comorbidity, by model, and age of screening cessation
	Comorbidity	Average comorbidity
	Model	MISCAN-Fadiaa	SPECTRUM^b
	Age of cessation =74 (vs 72)	0.9	0.7
	Age of cessation =76 (vs 74)	0.9	0.7
Harms
Braithwaite et al^Citation61		% of false-positive recalls at first mammography
Screening Group: First mammography for all	Comorbidity	Charlson score =0	Charlson score ≥1
	Ages: 66–74	8.6 (8.3–8.8)	8.9 (8.5–9.3)
	Ages: 75–89	8.0 (7.6–8.4)	8.8 (8.2–9.4)
Screening groups: Annual screening vs biennial screening		% of women with at least one false-positive recall after 10 years of subsequent mammography, by screening interval
		Annual		Biennial
	Comorbidity	Charlson score =0	Charlson score ≥1	Charlson score =0	Charlson score ≥1
	Ages: 66–74	49.7 (47.8–51.5)	48.0 (46.1–49.9)	30.2 (29.4–31.1)	29.0 (28.1–29.9)
	Ages: 75–89	47.2 (44.9–49.5)	48.4 (46.1–50.8)	26.6 (25.7–27.5)	27.4 (26.5–28.4)
Screening group: First mammography for all		% of false-positive biopsy recommendations at first mammography
	Comorbidity	Charlson score =0	Charlson score ≥1
	Ages: 66–74	1.2 (1.1–1.3)	1.7 (1.5–1.9)
	Ages: 75–89	1.2 (1.1–1.4)	1.7 (1.4–2.0)
Screening groups: Annual screening vs biennial screening		% of women with at least one false-positive biopsy recommendation after 10 years of subsequent mammography, by screening interval
		Annual		Biennial
	Comorbidity	Charlson score =0	Charlson score ≥1	Charlson score =0	Charlson score ≥1
	Ages: 66–74	9.8 (8.4–11.3)	11.8 (10.1–13.8)	4.6 (4.2–5.1)	5.6 (5.1–6.2)
	Ages: 75–89	9.2 (7.5–11.2)	11.3 (9.3–13.6)	4.1 (3.7–4.6)	5.1 (4.5–5.7)
Lansdorp-Vogelaar et al^Citation65	False-positive tests per 1,000 individuals screened according to guidelines since 50 years of age in populations with average comorbidity, by model, and age of screening cessation
Screening groups: Age of screening cessation	Comorbidity	Average comorbidity
	Model	MISCAN-Fadiaa	SPECTRUM^b
	Age of cessation 74(vs 72)	79	96
	Age of cessation 76(vs 74)	77	96
	Overdiagnosed cases per 1,000 individuals screened according to guidelines since 50 years of age in populations with average comorbidity, by model, and age of screening cessation
	Comorbidity	Average comorbidity
	Model	MISCAN-Fadiaa	SPECTRUM^b
	Age of cessation 74(vs 72)	0.8	0.5
	Age of cessation 76(vs 74)	1	0.6
Balance of benefits vs harms
Landsdorp-Vogelaar et al^Citation65	Number needed to screen to gain 1 life-year (NNS/LYG), by model and age of screening cessation
Screening groups: Age of screening cessation	Comorbidity	Average comorbidity
	Model	MISCAN-Fadiaa	SPECTRUM^b
	Age of cessation =74(vs 72)	132	173
	Age of cessation =76(vs 74)	146	198

Notes:

a MISCAN-Fadia: the MISCAN-Fadia model is a computer simulation program which incorporates information on the natural history of the disease as described by tumor stages and fatal tumor diameter (the size at which cancer becomes fatal) to construct models that compare the (cost-) effectiveness of different screening policies. It consists of four major components that simulate the demography and breast cancer incidence in the population, the natural history of a breast cancer tumor, the dissemination of screening mammography and its effects, and the dissemination of adjuvant treatment and its effects. bSPECTRUM: SPECTRUM is an event-driven continuous-time state model, which uses population-based estimates of breast cancer incidence and distribution of stage and other breast cancer characteristics (such as estrogen receptor status, response to treatment, and mortality) to estimate the efficacy of screening programs.

Abbreviations: CI, confidence interval; DCIS, ductal carcinoma in situ; LYG, life-years gained; NNS, number needed to screen; OR, odds ratio; RR, relative risk.

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