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Published online before print May 23, 2006, 10.1148/radiol.2401050170
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(Radiology 2006;240:33-38.)
© RSNA, 2006

Breast Imaging

Arterial Calcifications Seen on Mammograms: Cardiovascular Risk Factors, Pregnancy, and Lactation1

Angela H. E. M. Maas, MD, Yvonne T. van der Schouw, PhD, David Beijerinck, MD, Jan J. M. Deurenberg, MD, PhD, Willem P. T. M. Mali, MD, PhD and Yolanda van der Graaf, MD, PhD

1 From the Department of Cardiology, Isala Klinieken, Groot Wezenland 20, 8011 JW Zwolle, the Netherlands (A.H.E.M.M.); Julius Center for Health Sciences and Primary Care (Y.T.v.d.S., Y.v.d.G.), and Department of Radiology (W.P.T.M.M.), University Medical Center Utrecht, Utrecht, the Netherlands; and Preventicon Breast Cancer Screening Center, Utrecht, the Netherlands (D.B., J.J.M.D.). Received February 1, 2005; revision requested April 1; revision received April 14; accepted May 16; final version accepted August 25. Supported by research grant 2100.086 of ZonMw (Netherlands Organization for Health Research and Development). Address correspondence to A.H.E.M.M. (e-mail: A.Maas{at}diagram-zwolle.nl).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Purpose: To retrospectively assess if mammographic calcium deposits are related to coronary heart disease (CHD) risk factors and reproductive factors in a subset of women participating in the European Prospective Investigation into Cancer and Nutrition study.

Materials and Methods: The study was approved by the institutional review board of the University Medical Center Utrecht; informed consent was obtained. Mammograms were evaluated by two radiologists for the presence of breast arterial calcifications (BAC) in the Prospect cohort, a breast cancer screening population of women aged 49–70 years (mean, 57 years) within the European Prospective Investigation into Cancer and Nutrition study. Cardiovascular risk factors and reproductive factors were examined for independent effects on the prevalence of BAC. Logistic regression analysis was performed.

Results: BAC was present in 194 of 1699 (11%) women and increased with age to 20% in the highest quartile of age (mean, 66 years). The odds ratio was 4.7 in the highest versus the lowest quartile of age (95% confidence interval [CI], 2.9, 7.6). After adjustment for age, no significant association was found between BAC and traditional cardiovascular risk factors. Current smoking was inversely related to BAC (odds ratio, 0.6; 95% CI: 0.4, 0.9). BAC was prevalent in 2.5% of nulliparous women, in 9% of women with one or two children, and in 17% of women with three or more children (odds ratio, 7.2; 95% CI: 2.9, 18.0). Breast feeding after pregnancy was significantly associated with BAC in women who ever were pregnant (odds ratio, 2.2; 95% CI: 1.4, 3.6).

Conclusion: Calcifications in arteries on mammograms are associated with increasing age, pregnancy, and lactation but not with various cardiovascular risk factors.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Arterial calcification is a common feature of degenerative atherosclerotic disease, and its demonstration with modern imaging techniques provide insight into subclinical atherosclerosis (1–3). With conventional radiologic techniques such as mammography, calcium deposits in the arterial wall can be seen, but the cause and clinical importance of these calcifications is still unclear (4,5). Previously, we found a prevalence of breast arterial calcium (BAC) of 23% on mammograms of women at high risk for a coronary heart disease (CHD) event, whereas the prevalence of BAC was estimated at 9% in a low-risk population from a breast cancer screening program (6,7). Age, presence of diabetes mellitus, and number of pregnancies were found to be independently associated with BAC, but we were unable to identify other factors that were associated with BAC (6). To our knowledge, the association between pregnancy and arterial calcifications seen on mammograms has not been described before by others, and the association raises questions about the cause of BAC. Because bone metabolism is actively involved in both vascular calcification and pregnancy, we hypothesized that hormonal changes during pregnancy are important in the cause of calcifications in breast arteries (8–10).

Thus, the purpose of our study was to retrospectively assess if mammographic calcium deposits are related to CHD risk factors and to reproductive factors in the Prospect cohort, a subset of women participating in the European Prospective Investigation into Cancer and Nutrition study.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Population
The study population consisted of participants of the Prospect cohort, which is one of two Dutch contributions to the European Prospective Investigation into Cancer and Nutrition study. The total Prospect cohort consists of 17 357 women from a population-based breast cancer screening program who were enrolled between 1993 and 1997 in Utrecht and its surrounding areas. Women aged 49–70 years who were scheduled for breast cancer screening were invited to join the Prospect study, along with their invitation for routine mammography. Detailed information on the study population has been described elsewhere (11). At baseline, women filled in a general questionnaire, underwent a medical examination, and donated a 30-mL nonfasting blood sample. The blood sample was fractionated into serum, plasma, buffy coat, and erythrocyte aliquots. Prior to study inclusion, all women signed an informed consent form and gave permission for the use of their personal data and biologic material in substudies. The Prospect study and our current study were approved by the institutional review board of the University Medical Center Utrecht. For this study, we drew a 10% random sample (n = 1736) from which we collected the baseline mammograms and retrieved the frozen blood samples. We excluded 10 women for whom the baseline questionnaire was missing and 27 women for whom a blood sample was not available. Thus, our study population consisted of 1699 women (mean age, 57 years; range, 49–70 years).

Mammograms
All 1699 baseline mammograms (mediolateral oblique and craniocaudal views of both breasts) of participating women were obtained with a Senograph 600 or 800 unit (GE, Paris, France) and a screen-film combination (Min-R; Kodak, Chalon-sur-Saone, France). Two radiologists (D.B., J.J.M.D.) working independently, each with 18 years of mammography experience, retrospectively analyzed the mammograms for the presence of BAC with the criteria of Kemmeren et al (7).

Therefore, all mammograms were scored on the presence, location, and severity of arterial calcifications by each reader. There was disagreement in 85 of 1699 (5%) cases, and the two readers reviewed the mammograms together to reach a consensus. BAC was characterized by calcium deposits along the contours of the breast arteries on mammograms of the right, the left, or both breasts (Fig 1). The radiologists were blinded to the clinical data of the patients.


Figure 1
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  		Figure 1: Mediolateral oblique view of right breast shows arterial calcifications (arrows).

 
Cardiovascular Risk Factors
The general questionnaire contained questions on demographic characteristics such as reproductive history (number of pregnancies and miscarriages); previous (myocardial infarction or stroke) and current illnesses such as high blood pressure, diabetes mellitus, or hypercholesterolemia; and chronic disease risk factors, such as breast feeding, oral contraceptive use, hormone replacement therapy, smoking habits, alcohol consumption, physical activity, and family history. The physical examination included measurements of pulse rate, blood pressure, height, weight, and waist and hip circumferences. Systolic and diastolic blood pressures were measured in duplicate, and the mean value was calculated. Furthermore, height and weight were measured without shoes in light indoor clothing to compute body mass index, defined as weight divided by height squared (kilograms per square meter). Levels of serum total cholesterol and glucose were determined with the thawed blood samples by using an automated enzymatic procedure (Vitros 250; Johnson & Johnson, Rochester, NY).

Hypercholesterolemia was defined as present when a woman had a nonfasting total cholesterol level higher than 8.0 mmol/L (309 mg/dL) and/or when a woman reported that a physician had diagnosed hypercholesterolemia. Diabetes mellitus was defined as present when a woman had a nonfasting glucose level of more than 11.1 mmol/L (202 mg/dL) and/or when a woman reported that a physician had diagnosed diabetes mellitus. Hypertension was defined as measured systolic blood pressure higher than 160 mm Hg, a diastolic blood pressure higher than 95 mm Hg, and/or when a woman reported that a physician had diagnosed hypertension. Women were classified according to their smoking habits as current smokers or nonsmokers (ie, past smokers or never have been smokers). Previous myocardial infarctions and strokes were registered with self-report. Parity was defined as all pregnancies, including spontaneous abortions. Breast feeding was defined as having breast fed at least one child.

Statistical Analysis
Baseline characteristics (age, previous myocardial infarction, stroke, hypertension, diabetes mellitus, hyperlipidemia, smoking, reproductive history, body mass index, and glucose and lipid levels) were expressed according to the presence or absence of BAC (A.H.E.M.M., Y.T.v.d.S., Y.v.d.G.). Means and standard deviations were computed for continuous variables, and frequency distributions were computed for categorical variables. Risk factors for cardiovascular disease (age, body mass index, blood pressure, diabetes mellitus, smoking, and hyperlipidemia) and reproductive factors (parity, breast feeding, oral contraceptive use, and hormone replacement therapy use) were examined for independent effects on the prevalence of BAC. The associations between CHD risk factors and reproductive factors with BAC were assessed by using logistic regression analysis and are expressed as odds ratios with 95% confidence intervals (CIs). We adjusted for age by entering age as a continuous variable in the regression model. All analyses were carried out with statistical software (SPSS 11.0 for Windows; SPSS, Chicago, Ill).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Baseline characteristics of the study group participants with and participants without BAC are shown in Table 1. BAC was present in 194 (11%) participants. The prevalence of BAC increased with advancing age, from 22 of 426 (5%) participants in the first quartile (mean age, 50 years), to 28 of 459 (6%) participants in the second quartile (mean age, 54 years), to 59 of 432 (14%) participants in the third quartile (mean age, 60 years), and to 85 of 419 (20%) participants in the fourth quartile (mean age, 66 years). The odds ratio was 4.7 in the highest versus the lowest quartile of age (95% CI: 2.9, 7.6)


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  		Table 1. Prevalence of Risk Factors in 1699 Participants with and Participants without BAC

 
CHD Events and Risk Factors
The number of previous CHD events (n = 29) and cases of diabetes mellitus (n = 22) was too rare in this low-risk population to estimate relationships with BAC. BAC was significantly less prevalent in current smokers (26 of 398 [7%] women) when compared with that of nonsmokers (168 of 1329 [13%] women) (P < .001). Body mass index of more than 25 kg/m2 was not associated with BAC. The prevalence of BAC was slightly higher in participants with known hypertension (45 of 350 [13%] participants vs 149 of 1377 [11%] participants), but mean systolic blood pressure was not different between both groups. Mean serum glucose levels were not different between women with and women without BAC. When odds ratios were adjusted for age, the associations with hypertension, serum glucose levels, and lipid parameters were not significantly associated with BAC.

Reproductive Factors
The prevalence of BAC was significantly associated with previous pregnancies (P < .001) and breast feeding (P < .001). All but five of 194 (97%) women with BAC had been pregnant. Seventy-six of 194 (39%) women with BAC had one or two children, and 112 of 194 (58%) women with BAC had three or more children. The prevalence of BAC increased from five of 205 (2.4%) cases in women without children to 76 of 845 (9%) cases in women with one or two children (odds ratio, 4.8; 95% CI: 1.9, 12.0) and to 112 of 676 (17%) cases in women with three or more children (odds ratio, 7.2; 95% CI: 2.9, 18.0) (Table 2). The age-adjusted odds ratio for parous versus nulliparous women was 5.3 (95% CI: 2.2, 13.2). The prevalence of BAC among women who breast fed after pregnancy (1191 of 1521 women [78%]) was 166 of 1191 (14%) women, compared with 22 of 330 (7%) women who had never breast fed (odds ratio, 2.2; 95% CI: 1.4, 3.6). Women who had used hormone replacement therapy had a nonsignificant lower prevalence of BAC (34 of 427 [8%] women), compared with those who had never used hormone replacement therapy (160 of 1300 [12%] women). There was no relation between previous or current oral contraceptive use and BAC.


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  		Table 2. Age-adjusted Odds Ratios of BAC

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In this cohort of women aged 49–70 years from a breast cancer screening program, we found a BAC prevalence of 11%. The strongest determinants of BAC were parity (odds ratio, 5.3) and breast feeding (odds ratio, 2.2), which suggests that the calcium deposits may be due to changes during pregnancy and breast feeding rather than to CHD risk factors. Although there was a wide spread in the distributions of blood pressure, cholesterol levels, and glucose levels, after adjustment for age, these risk factors were not found to be related to BAC.

Thus far, mammographic arterial calcifications have been attributed to medial sclerosis of the breast arteries. Medial sclerosis is comparable to Mönckeberg medial sclerosis, which is often seen in the smaller peripheral vessels of older patients with diabetes mellitus (4,12,13).

Vascular calcification is currently considered a regulated process with mechanisms similar to bone formation and with a diversity of locations and morphology of the calcified deposits (8,9,14,15). Bonelike tissues have been found in atherosclerotic lesions, medial sclerosis, and valvular stenosis (16–18). The appearance of calcium in different vascular beds occurs 10–15 years later in women than in men (19). In pathologic studies, medial calcification differs from intimal calcification in the absence of signs of inflammation and lipid deposits (20,21). With conventional x-ray techniques, it is not possible to differentiate with certainty between intimal and medial calcifications, although the appearance of medial calcifications is more fine and diffuse in smaller vessels, compared with the large and discontinuous appearance of intimal calcifications in large and medium-sized arteries (13).

In the peripheral vessels of diabetic patients, medial sclerosis and calcifications are an independent predictor of CHD events and severe peripheral artery occlusive disease (22). In a previous breast cancer screening cohort of 12 239 women, we found a higher prevalence of BAC in diabetic patients (15.4%) compared with that of nondiabetic patients (9%), and mortality in diabetic patients with BAC was 74% higher than that of diabetic patients without BAC. In another study in 600 women with a high risk for diabetes, we found a 58% greater risk of BAC in those with diabetes compared with the risk of BAC in those without diabetes (odds ratio, 1.58) (6).

Hyperglycemia may be related to medial calcium deposits by regulating the production of osteogenic proteins, such as osteoprotegerin, matrix Gla protein, osteocalcin, and others (14,17,21–23). Variations in gene expression of these proteins can change vascular smooth muscle cells into a more osteogenic phenotype (Fig 2). In women with diabetes and subsequent cardiovascular complications, serum osteoprotegerin levels were found to be higher compared with those of the control group (23). We assume that in our present study of relatively healthy women from a breast cancer screening program, the prevalence of diabetes mellitus and mean serum glucose levels were too low to enhance medial vascular calcification. The reason for the lower prevalence of mammographic calcium found in current smokers is unclear.


Figure 2
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  		Figure 2: Mechanism of calcification in breast arteries.

 
Microcalcifications at mammography have been reported in a recent lactating woman, but, to the best of our knowledge, our study is the first to date to describe an association between calcifications in the arteries on mammograms and reproductive factors (24). Given the strong associations we found between pregnancy and breast feeding and BAC, we assume that calcium deposits in breast arteries may be caused by transient hypercalcemia, which is induced by pregnancy and breast feeding. Pregnancy is associated with major changes in calcium metabolism to meet the high requirements for fetal growth and for breast-milk production (10). Some biochemical proteins of bone resorption and formation (eg, osteocalcin, bone morphogenic protein) are elevated in the first months of lactation and are also found in calcified vascular tissues (25,26). In response to calcifying and atherosclerotic stimuli, vascular smooth muscle cells of the arterial wall can migrate and dedifferentiate into cells with osteocytic and chondrogenic changes in gene expression (25,27). We hypothesize that when calcium (hydroxyapatite) is more available in the breast circulation, as occurs during pregnancy and lactation, vascular smooth muscle cells can become activated and promote mineralization (Fig 2). A comparable linkage of vascular and cardiac valve calcification and osteoclastic resorption in the skeleton has been found in women after menopause (28,29). These findings are in line with the observations that premenopausal women and women who use hormone replacement therapy have a lower content of calcium in the coronary arteries, as well as in the breast arteries, suggesting that lack of estrogens is important in the calcification of the arterial wall (19,30–32).

Limitations of our fairly small study of relatively young women from a breast cancer screening program are the low prevalence of diabetes mellitus and previous CHD events and a lower extent of calcium deposits that is inherent to younger age. We were able to provide, however, detailed information on the reproductive history of the participants, as well as on CHD risk factors, which we could assess due to the combination of self-report and measured values.

In conclusion, we found that mammographic arterial calcifications are associated with increasing age, pregnancy, and lactation but not with traditional cardiovascular risk factors. Thus far, it is not known whether pregnancy and lactation may have a role in calcification of other vascular beds besides breast arteries.


   FOOTNOTES
 

Abbreviations: BAC = breast arterial calcium • CI = confidence interval • CHD = coronary heart disease

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, A.H.E.M.M., D.B., J.J.M.D., Y.v.d.G.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, A.H.E.M.M., Y.T.v.d.S., W.P.T.M.M., Y.v.d.G.; clinical studies, A.H.E.M.M., Y.v.d.G.; experimental studies, D.B., J.J.M.D.; statistical analysis, A.H.E.M.M., Y.T.v.d.S., W.P.T.M.M., Y.v.d.G.; and manuscript editing, A.H.E.M.M., Y.T.v.d.S., D.B., W.P.T.M.M., Y.v.d.G.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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