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Abstract
Late-stage diagnosis of breast cancer is associated with poor survival. Identification of individuals at high risk of late-stage diagnosis
could be an effective step to reduce breast cancer mortality. We examined the association of socio-demographic factors and health behav-
ior with breast cancer stage in a population-based sample of 380 female breast cancer patients in Saarland, Germany. Overall, 182 women
(47.9%) were diagnosed with late-stage (regional or distant) breast cancer. After control for potential confounding by multivariate logis-
tic regression, an increased risk of late-stage diagnosis was observed for older age (OR 1.8; 95% CI 1.0–3.2), foreign nationality (OR
3.9; 95% CI 0.7–20.8), living in large households (OR 1.7; 95% CI 1.0–2.9), non-participation in general health check-up (OR 1.5;
95% CI 0.9–2.4) and low interest in health care (OR 1.6; 95% CI 1.0–2.7). The proportion of late-stage cancer was clearly decreased
when tumors were detected by screening (OR 0.4; 95% CI 0.2–0.8). Certain socio-demographic factors and characteristics of health be-
havior seem to represent independent risk indicators of late-stage diagnosis. © 2001 Elsevier Science Inc. All rights reserved.
Keywords: Breast neoplasm; Neoplasm staging; Socio-demographic factors; Health behavior; Diagnostic delay
stage at diagnosis in a population-based sample of breast “Localized” disease included all cases with T1–T3 and N0
cancer patients in Saarland, Germany, diagnosed between and M0, “regional” included all M0 and N1 or M0 and T4
October 1996 and February 1998. and “distant” comprised all cases with M1. Although this is
a relatively simple staging scheme, it has clear prognostic
significance and is widely used in cancer epidemiology. For
2. Materials and methods
the present study the relatively small number of “distant”
2.1. Study design disease (n 14) was combined with “regional” (n 168)
to represent late-stage disease in contrast to early (localized)
This study is based on data obtained from the VERDI-
disease.
study (“Verlauf der diagnostischen Abklärung bei Krebs-
erkrankungen”), a population-based study among patients 2.4.2. Socio-demographic factors
with primary breast, gastric or colorectal cancer from Saar- Socio-demographic factors included age ( 50 years,
land, Germany, to assess the course from the first symptoms 50–65 years, 65 years), nationality (German, foreign),
to diagnosis and treatment. Saarland is a state in southwest place of residence (population 100,000, 100,000), edu-
Germany close to the French border, covering a population cation (10 years, 10 years), current employment status
of 1.08 million inhabitants. (employed, unemployed, housewife/retired), most recent
occupation (blue collar, white collar, never worked), kind of
2.2. Study population
health insurance (private, non private), living arrangements
The target population comprised all female breast cancer [lives alone, lives with spouse only, lives with spouse and
patients from Saarland, aged 18–80 years, with histologi- others, lives with others (not spouse)].
cally confirmed invasive breast cancer diagnosed between
October 1, 1996 and February 28, 1998. Patients with recur- 2.4.3. Indicators of health behavior
rent disease at the time of the interview, who died before the Indicators of health behavior included regular monthly
interview, who were not fully informed about their breast breast self- examination (yes, no), utilization of breast cancer
cancer diagnosis, or with no or only little German language screening (clinical breast examination or mammography) and
skills were excluded. Eligible patients were reported to the of general health check-up during past 5 years (yes, no) and
study center by their physicians after they had given in- interest in health issues (low, regular). The biennial general
formed consent. All hospitals from the Saarland and from health check-up to screen for diabetes mellitus, renal and
all adjacent counties from the Rhineland-Pfalz participated chronic vascular diseases is offered to all members of regular
in case identification and enrollment. Overall, 387 of 401 health insurance plans aged 36 years and older in Germany
eligible women reported to the study center with breast can- since 1989. A proxy measure of interest in health issues was
cer could be recruited (reponse rate 96.5%), representing defined by the number of sources reported by the respondent
approximately 50% of all new incident cases during the re- to inform herself about health issues before the current dis-
cruitment period according to projections by the Saarland ease became apparent. The list of sources included TV, radio,
Cancer Registry. The study participants did not substan- newspapers, books, information booklets provided by health
tially differ from the source population in terms of basic so- insurances, friends or relatives, pharmacists, physicians and
cio-demographic characteristics with the exception of a other sources. The lowest tertile ( 3 sources) was consid-
slightly higher proportion of younger patients. ered to represent low interest in health issues.
Table 1 Table 1
Description of study population (n 380) Continued
n % n %
a
Socio-demographic characteristics Duration of symptoms and diagnostics
Age (years) 0–1 months 189 49.7
50 101 26.6 1–3 months 92 24.2
50–65 168 44.2 3 months 99 26.1
65 111 29.2 a
Nationality Defined as “interval between first symptom or screening examination
German 370 97.4 and definite diagnosis.”
Foreign 10 2.6
Size of town (number of citizens) of the above- mentioned conditions during the last year be-
Small (100.000) 337 88.9 fore onset of breast cancer symptoms. The list of medical
Large (100.000) 42 11.1
conditions was constructed according to Moritz and Satari-
Education
10 years 285 75.2 ano [32] and comprises medical conditions where an exami-
10 years 94 24.8 nation of the chest is likely to occur.
Current employment status
Housewife/retired 239 63.2 2.4.5. Mode of detection of tumor
Employed 121 32.0 Mode of detection of tumor (symptoms, incidental find-
Unemployed 18 4.8 ing, screening) and duration of symptoms and diagnostics
Last occupational class
(interval between first symptom or screening examination
White collar 215 57.6
Blue collar 67 18.0 and definite diagnosis, categorized as 1 month, 1–3
Never worked 91 24.4 months, 3 months) were obtained from the patient. Both
Health insurance variables might be considered as potential intermediate
Non private 336 88.7 variables in the association between socio-demographic fac-
Private 43 11.3
Living arrangements
tors and stage of disease at diagnosis.
Single 99 26.1
2.5. Statistical methods
With spouse only 136 35.9
With spouse and others 96 25.3 Bivariate associations between stage of disease and each
With others (not spouse) 48 12.7 of the socio-demographic, health, social and potential inter-
Health behavior mediate variables were examined using contingency tables
Regular monthly breast self examination and chi-square statistics. Crude odds ratios (OR) including
Yes 197 54.0
No 168 46.0
95% confidence intervals (CI) were calculated with logistic
Breast cancer screening during past 5 years regression. Next, logistic regression models were developed
Yes 284 74.9 to examine the simultaneous influence of all socio-demo-
No 95 25.1 graphic and health behavior factors on the likelihood of be-
General health check-up during past 5 years
Yes 234 62.1
ing diagnosed with late-stage breast cancer. The first model
No 143 37.9 (model 1) assessed the joint effect of all listed socio-demo-
Interest in health issues graphic factors. Model 2 examined whether sociod-demo-
Regular 270 71.1 graphic factors are associated with breast cancer stage inde-
Low 110 28.9
pendently from health behavior, health characteristics and
Health characteristics, family history
Body mass index family history. To check whether the observed association
25 kg/m2 167 45.5 between socio-demographic factors, health behavior and
25–30 kg/m2 110 30.0 breast cancer stage was attributable to a long symptomatic
30 kg/m2 90 24.5 period, the third model further considered information re-
Comorbidity
Yes 256 67.4
garding duration of symptoms and diagnostics. A final
No 124 32.6 model containing only the most predictive variables was ob-
History of benign mastopathy tained by stepwise selection processing (significance level
Yes 89 23.4 for staying or entering in the model both equal 0.15).
No 291 76.6
Family history of breast cancer
Yes 51 13.4 3. Results
No 329 86.6
Hormones (OC, HRT) during past year 3.1. Study population
Yes 112 29.7
No 265 70.3 From 387 women with primary breast cancer, seven had to
Tumor detected by be excluded due to missing data on stage, leading to a final
Symptoms 287 75.5
Screening 67 17.6 study population of 380 women. Characteristics of the study
Incidental finding 26 6.8 sample are shown in Table 1. The mean age of the study pop-
ulation was 58.0 years. Most study participants were of Ger-
(Continued)
722 V. Arndt et al. / Journal of Clinical Epidemiology 54 (2001) 719–727
Table 2 Table 2
Percentages of cases with late stage Continued
Health insurance and education were not related to stage of but did not substantially change the risk estimates for late-
disease. Older patients (age 50 years) tended to present at stage diagnosis of the socio-demographic variables.
later stage, but the differences were marginal. Among the variables describing health behavior, low in-
A stronger association with breast cancer stage was seen terest in health issues (OR 1.7, 95% CI 1.0–2.9) and lack
among variables describing health behavior. Low interest in of general health check-ups during the past 5 years (OR
health issues was clearly related with late-stage diagnosis of 1.6, 95% CI 1.0–2.7) were independently associated with
breast cancer. Attending a general health check-up during late-stage breast cancer. A previous history of clinical or
the past 5 years was associated with a higher proportion of self-conducted breast cancer screening was not associated
localized tumors. Although breast cancer stage was less ad- with favorable breast cancer stage in multivariate analysis.
vanced among patients who attended breast cancer screen- Obesity (BMI 30 kg/m2) was associated with late-stage
ing in the past, the association between history of profes- breast cancer independently from socio-demographic char-
sional breast cancer screening and actual stage of disease acteristics and health behavior.
was weak and statistically non-significant. No difference in Further adjustment for type of detection and total diag-
stage of breast cancer was seen between women who re- nostic delay had only little impact on the risk estimates re-
ported to check their breasts regularly compared to others. ferring to socio-demographic and health behavior variables.
There was a tendency that breast cancer stage was less Although the association between tumor detection by
often advanced in lean women (BMI 25 kg/m2), women screening and tumor stage is slightly attenuated in the multi-
who have seen a doctor for treatment of some other chronic variate regression model, screening was the strongest pre-
disease during the last year before diagnosis and among dictor of early-stage even after adjusting for all socio-demo-
women with a first-degree relative with breast cancer. The graphic and health behavior variables. In contrast, no
association between comorbidity and stage of breast cancer significant association between tumor stage and duration of
diagnosis was not uniform for all underlying conditions. symptoms and/or diagnostic work-up was seen in the multi-
The proportion of women with advanced-stage breast can- variate regression model. Education, place of residence,
cer was lower than average among women with ischemic marital status, health insurance and recent use of hormones
heart disease (44.9%), stroke (38.5%), asthma (44.4%), ob- were not associated with stage of disease in any model.
structive lung disease (42.9%), arthritis (41.9%) or other Results of multivariate analysis when restricted to the
cancer (41.7%) but higher for women with diabetes (48.7%) most predictive variables of late-stage diagnosis are shown
or hypertension (50.8%, data not shown). The use of hor- in Table 4. Besides screening as the most influential predic-
mones (OC, HRT) was not associated with stage of disease. tor of stage of diagnosis, older age, foreign nationality, liv-
The type of detection was strongly associated with stage ing in large households, lack of general health check-ups
of breast cancer at diagnosis. In general, stage of breast can- during the past 5 years, low interest in health issues, BMI
cer was much more favorable among those women whose 30 kg/m2, history of benign mastopathy and family his-
tumors were detected during the course of a regular screen- tory of breast cancer were strongly associated with late-
ing examination. No difference in tumor stage was noticed stage disease. Both age and living arrangements could be di-
between tumors detected by symptoms and those detected chotomized without loss of information since the risk esti-
incidentally. The duration of symptoms and diagnostic mates of the referring subcategories did not differ (P
work-up was positively associated with tumor stage, how- 0.90). With an area under the receiver operating characteris-
ever the differences were of limited magnitude and not sta- tic (ROC) curve of 0.68 the explanatory capacity of this par-
tistically significant. simonious model was quite high.
Table 3
Crude and adjusted odds ratios (including 95% confidence intervals) of late-stage breast cancer (distant/regional versus localized)
Crude OR Model 1 Model 2 Model 3
Socio-demographic characteristics
Age
50–65 years 1.2 (0.7-1.9) 1.7 (0.9-3.1) 1.8 (0.9-3.5) 1.9 (1.0-3.8)
65 years 1.2 (0.7-2.1) 2.2 (1.0-4.8) 1.9 (0.8-4.5) 2.0 (0.8-4.9)
Foreign nationality 2.6 (0.7-10.2) 2.2 (0.5-9.4) 3.3 (0.6-18.1) 3.2 (0.6-18.1)
Size of town 100,000 1.5 (0.8-2.9) 1.4 (0.7-2.8) 1.1 (0.5-2.5) 1.1 (0.5-2.5)
Education 10 years 0.9 (0.6-1.4) 1.0 (0.6-1.7) 1.0 (0.5-1.8) 0.9 (0.5-1.7)
Employment status
Employed 1.1 (0.7-1.7) 1.6 (0.9-2.8) 1.4 (0.8-2.6) 1.4 (0.8-2.7)
Unemployed 1.8 (0.7-4.8) 2.3 (0.8-7.1) 1.7 (0.5-5.4) 1.6 (0.5-5.4)
Occupational class
Blue collar 1.3 (0.7-2.2) 1.4 (0.8-2.4) 1.3 (0.7-2.4) 1.2 (0.6-2.3)
Never worked 1.4 (0.9-2.3) 1.6 (0.9-2.9) 1.9 (1.0-3.6) 1.9 (1.0-3.6)
No private health insurance 1.2 (0.6-2.3) 1.2 (0.6-2.5) 1.5 (0.7-3.1) 1.4 (0.7-3.1)
Living arrangements
Single 1.3 (0.8-2.1) 1.1 (0.6-2.0) 1.1 (0.6-2.1) 1.1 (0.6-2.1)
With spouse and others 1.7 (1.0-2.4) 2.0 (1.1-3.6) 1.9 (1.0-3.5) 1.9 (1.0-3.5)
With others (not spouse) 1.2 (0.6-2.4) 1.2 (0.6-2.4) 1.2 (0.6-2.7) 1.2 (0.6-2.7)
Health behavior
No regular monthly breast self examination 1.0 (0.6–1.5) — 1.1 (0.7–1.7) 1.0 (0.6–1.7)
During past 5 years
No breast cancer screening 1.2 (0.8–1.9) — 1.0 (0.6–1.8) 0.9 (0.5–1.7)
No general check-up 1.5 (1.1–2.8) — 1.6 (1.0–2.7) 1.5 (0.9–2.6)
Low interest in health issues 1.8 (1.1–2.8) — 1.7 (1.0–2.9) 1.7 (1.0–2.8)
Health characteristics, family history
Body mass index
25–30 kg/m2 1.4 (0.9-2.3) — 1.3 (0.7-2.3) 1.4 (0.8-2.5)
30 kg/m2 1.7 (1.0-2.8) — 1.7 (0.9-3.2) 1.8 (0.9-3.3)
Comorbidity 0.7 (0.5-1.1) — 0.9 (0.5-1.5) 0.9 (0.5-1.6)
History of benign mastopathy 1.2 (0.8-2.0) — 1.6 (0.9-2.7) 1.5 (0.8-2.7)
Hormones during past year 1.0 (0.6-1.5) — 1.1 (0.6-1.9) 1.2 (0.7-2.2)
Family history of breast cancer 0.7 (0.4-1.2) — 0.6 (0.3-1.1) 0.6 (0.3-1.2)
Tumor detected by
Screening 0.4 (0.2-0.7) — — 0.4 (0.2-0.9)
Incidental finding 1.1 (0.5-2.5) — — 1.2 (0.5-2.9)
Duration of symptoms and diagnostics
1–3 months 1.3 (0.8–2.1) — — 0.9 (0.5–1.7)
3 months 1.5 (0.9–2.4) — — 1.4 (0.8–2.5)
Model Fitting (likelihood ratio) 2 15.4 2 32.4 2 41.5
13 df 23 df 27 df
P 0.28 P 0.09 P 0.04
Association of predicted probabilities and observed responses c 0.609 c 0.675 c 0.692
Reference categories: age 50 years; nationality German; size of town 100,000; education 10 years; employment status housewife/retired; occu-
pational class white collar; health insurance private; living arrangements lives with spouse only; monthly breast examination; breast cancer screening
yes; general check-up yes; interest in health issues regular; body mass index 25.0 kg/m2; comorbidity no; history of benign mastopathy no; hor-
mones no; family history of breast cancer no; tumor detected by symptoms; duration of symptoms and diagnostics 1 month.
toms might be attributed to comorbid conditions, but our It is noteworthy that these socio-demographic factors
data indicate that old age is associated with late-stage diag- seem to represent independent risk indicators of late-stage
nosis of breast cancer independently from comorbidity. diagnosis irrespective of health behavior and health aware-
Language or cultural barriers may impede women from eth- ness. The data also show that intention to seek evaluation of
nic minorities to seek medical advice. breast symptoms is not merely a matter of education and
We also found that women who live in larger households economics. According to Facione [42], it is dependent on a
and thus may have to care for children or other dependent per- complex picture of personal and social factors, on the per-
sons are at higher risk to present with late-stage breast cancer. ceived amount of negative consequences of delaying diag-
To our knowledge, the association between living arrange- nosis and on previous habits of health care utilization.
ments and late-stage diagnosis has not been observed so far, Besides socio-demographic characteristics, factors repre-
but Moritz and Satariano [32] found that women who lived senting health behavior and health awareness, such as inter-
alone were least likely to be diagnosed with advanced disease. est in health issues or attending general check-up examina-
V. Arndt et al. / Journal of Clinical Epidemiology 54 (2001) 719–727 725
Table 4 past 5 years prior to the onset of the current disease, this fa-
Final model predicting late stage diagnosis of breast cancer vorable association did not persist in multivariate analysis.
OR (95% CI) One explanation could be that women who had inconspicu-
Socio-demographic characteristics ous mammographies in the recent past might tend to neglect
Age 50 years 1.8 (1.0–3.2) self-discovered symptoms which will delay early detection
Foreign nationality 3.9 (0.7–20.8)
Lives with spouse and others 1.7 (1.0–2.9)
of the tumor. Another explanation could be that the staging
Health behavior scheme we used is too crude to detect differences in tumor
During past 5 years no general check-up 1.5 (0.9–2.4) size, especially among women where the tumor is confined
Low interest in health issues 1.6 (1.0–2.7) to the breast. However, observational studies which exam-
Health characteristics, family history
ined the association between previous mammography use
Body mass index
25-30 kg/m2 1.4 (0.8–2.4) and breast cancer stage are equivocal. Taplin et al. [47] re-
30 kg/m2 1.8 (1.0–3.2) ported a reduction in late-stage disease occurred among
History of benign mastopathy 1.6 (0.9–2.7) women 50 years of age and older, who underwent regular
Family history of breast cancer 0.6 (0.3–1.2) mammography, even when regular was not synonymous
Tumor detected by
Screening 0.4 (0.2–0.8)
with annual. In contrast, a recent study from Italy has shown
Model Fitting that previous mammographies are not uniformly related to
likelihood ratio 2 33.8, 10 df stage and that health-aware women who did not undergo
P 0.0002 regular mammography have a relatively short diagnostic de-
Association of predicted probabilities c 0.682
lay if they develop signs of breast cancer [27].
and observed responses
Monthly breast self-examination (BSE) to decrease mor-
Reference categories: age 50 years; nationality German; living ar- tality from breast cancer is frequently advocated. However,
rangements: all others; interest in health issues regular; body mass in-
dex 25.0 kg/m2; tumor detected by symptoms or incidental finding.
evidence for the value of BSE is limited. None of the major
randomized screening studies has produced data on the ef-
fectiveness of BSE in reducing mortality from breast cancer
tions, seem to be strong and independent predictors of [48–51]. The results suggest that BSE as practiced by most
tumor stage. Women who are interested in health issues and women in our study population is of little or no benefit de-
who volunteer for regular screening are more likely to be spite the observation that over 75% of all breast cancers
aware of their health and motivated to present promptly if were discovered by the women themselves.
they develop breast cancer symptoms [43]. Neither education nor comorbidity were related to stage
Early diagnosis of breast cancer can either result from at diagnosis within our study population. Former reports in-
screening of asymptomatic patients or from patients with dicated that women with low education tend to present at
symptoms who present to a doctor in a timely manner. The later stage [21,52], but the difference might be too small to
favorable outcome with respect to stage at diagnosis among be detected in our study. The association between comor-
asymptomatic patients whose tumors have been discovered bidity and stage of diagnosis was not uniform for all condi-
in the course of a screening examination is obvious. Our tions and its interaction with diagnostic decision making de-
data furthermore indicate that a short duration of symptoms serves further study. Women with comorbid conditions may
and a timely diagnostic work-up is also compatible with an be more likely to see a physician but non-specific cancer
early stage at diagnosis. symptoms like fatigue might also be attributed to comorbid
The finding that obese women are at higher risk of late- conditions.
stage diagnosis is in agreement with several studies which Weak, statistically non-significant associations were
reported an association between increasing body mass index found with respect to employment status or occupational
(BMI) or body weight and advanced stage [29,44,45]. De- class. Patient delay among low SES women has been ad-
tection of a tumor is more difficult among women with dressed in several studies [53–56] without finding sufficient
larger breasts and it is generally assumed that increased evidence. Regular health insurance companies, who insure
BMI is a proxy measure for increased breast size. The find- 89% of the population in Germany, promote and cover atten-
ing that women with a first-degree relative with breast can- dance of cancer screening measures. Despite this encourage-
cer are less likely to be diagnosed with late-stage cancer is ment, our data suggest that privately insured patients tend to
likely to be due to higher breast cancer awareness, as sug- present at an earlier stage than members of regular health in-
gested by Berman and Wandersman [46]. These women surances. Members of private health insurances tend to be
might be more susceptible to seek help if they discover wealthier, younger and better educated. Due to the lack of
signs of breast cancer [44]. power our results do not allow firm conclusions about the as-
The finding that neither previous history of breast self-ex- sociation between type of health insurance and tumor stage.
amination nor clinical breast cancer screening are associated This study has examined a range of individual factors that
with breast cancer stage is somewhat surprising. Although might influence breast cancer stage at time of diagnosis. To
the proportion of late-stage breast cancer cases was lower in our knowledge, this work is unique in looking simulta-
women who underwent breast cancer screening during the neously at socio-demographic, health behavior and other re-
726 V. Arndt et al. / Journal of Clinical Epidemiology 54 (2001) 719–727
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man Cancer Aid Foundation, M24/95/BR I). The authors
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