The European Journal of Public Health Advance Access originally published online on July 28, 2005
The European Journal of Public Health 2005 15(6):627-633; doi:10.1093/eurpub/cki037
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Health Inequalities |
Sex differences in the associations of socioeconomic status with undiagnosed diabetes mellitus and impaired glucose tolerance in the elderly population: the KORA Survey 2000
W. Rathmann1, B. Haastert1, A. Icks1, G. Giani1, R. Holle2, C. Meisinger3, A. Mielck2 The KORA Study Group
1 Institute of Biometrics and Epidemiology, German Diabetes Center, Heinrich Heine University, Düsseldorf, Germany
2 Institute of Health Economics and Health Care Management, GSF, National Research Centre for Environment and Health, Neuherberg, Germany
3 Institute of Epidemiology, GSF, National Research Centre for Environment and Health, Neuherberg, Germany
Correspondence: Dr Wolfgang Rathmann MSPH, German Diabetes Center, Auf'm Hennekamp 65, D-40225 Düsseldorf, Germany, tel: +49 211 3382 663, fax: +49 211 3382 677, e-mail: rathmann{at}ddfi.uni-duesseldorf.de
Received January 9, 2004, accepted July 28, 2004
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Background: Sex differences in the associations of socioeconomic status (SES) with prevalence of undiagnosed diabetes mellitus, impaired glucose tolerance (IGT) and known risk factors of type 2 diabetes mellitus were investigated in an elderly population. Methods: Oral glucose tolerance tests were carried out in 1354 randomly selected subjects (697 men, 657 women) aged 55–74 years in the population-based KORA Survey 2000, Augsburg, Germany. Odds ratios (ORs) and 95% confidence intervals (CIs) for undiagnosed diabetes or IGT by education, occupation and income were estimated using logistic regression controlling for age, waist circumference, blood pressure, triglycerides, physical activity, smoking and alcohol intake. Results: All three SES variables were significantly inversely related to body mass index, waist circumference and low physical activity in women (P < 0.05). In men, these associations were weaker or absent. Using the lowest category as reference, occupational status was significantly associated with undiagnosed diabetes in women (adjusted OR 0.5; 95% CI 0.3–0.8) after controlling for risk factors in multivariate regression. The OR was also reduced with higher income in women (adjusted OR, diabetes: 0.7; 95% CI 0.5–1.03). Among men, no significant relations of the SES indicators with unknown diabetes were observed. However, the odds of having IGT was lower with higher occupational status in men (adjusted OR 0.7; 95% CI 0.5–0.9). Conclusions: Undiagnosed type 2 diabetes was related to low SES defined by occupation or income in women only. In men, low occupational status was independently associated with higher IGT risk. Educational level was not related to glucose disorders in both sexes in the elderly population.
Keywords: diabetes mellitus, impaired glucose tolerance, obesity, socioeconomic status
Socioeconomic status (SES) is inversely associated with the prevalence of type 2 diabetes mellitus in industrialized countries including the USA,1–3 Canada,4–6 the UK,7–11 Sweden,12 The Netherlands13 and Germany.14,15 This relationship has also been found in specific ethnic groups with high diabetes risk.16,17 Furthermore, the risk of developing diabetes over time was related to SES.18 The association between social circumstances and risk factors of type 2 diabetes, i.e. insulin resistance, may start in childhood.19,20 Although in most populations only half of all cases are diagnosed, the majority of these studies were based on self-reports and thus did not differentiate between known and previously unknown diabetes.21
The health impact of social status may not be the same in men and women. Only a few studies have assessed sex differences in the relationship between SES and diabetes.1,4,16 In national surveys in the USA and Canada, SES was more closely associated with diabetes in women than in men.1,4 The pathways by which SES may differently affect the development of type 2 diabetes in men and women are unclear.1
Currently, only one study has investigated the relationship between SES and impaired glucose tolerance (IGT), and reported no significant association.22 IGT is a risk factor for type 2 diabetes and coronary heart disease.23 Obesity, the major predictor of IGT and type 2 diabetes, is more prevalent in groups of lower SES, in particular, among women.24
The impact of abdominal obesity, which is closely linked with insulin resistance, on the association between SES and glucose intolerance has rarely been studied.25–27
In order to fill some of these gaps, the aims of this study were to assess the sex-specific associations of SES, defined by education, occupation and income, with undiagnosed diabetes, IGT and known risk factors of type 2 diabetes mellitus, using data from a population-based survey in Augsburg, Germany.
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Study population
The KORA Survey 2000 (KORA: Cooperative Health Research in the Region of Augsburg) is a population-based study in Southern Germany using the same region and methods as the WHO MONICA project.28 Subjects were invited to participate from the city of Augsburg and 16 towns and villages out of 70 communities from the surrounding districts, which had about 600 000 inhabitants in 1999. Within each selected community, a stratified sample with 10 equal strata by gender and age was drawn; four of these strata included male and female subjects aged 55–74 years (two-stage cluster sampling).
Overall, 1653 (62%) of 2656 subjects aged 55–74 years participated. Non-participants (n = 911) were either too ill to come to the study centre (n = 145), had no time to attend investigations (n = 78) or were in general unwilling to participate (n = 651) despite enormous efforts to increase participation rate. After excluding 131 participants with known diabetes and further drop-outs, which were mainly persons who were not able to attend the fasting investigation during morning hours [non-fasting, n = 158; technical problems, n = 8; vomiting during oral glucose tolerance tests (OGTT), n = 2; missing 2 h glucose, n = 1], 1354 subjects had an OGTT.28
Fasting OGTTs were performed after informed consent in participants aged 
55 years without known diabetes from October 1999 to April 2001. Standardized OGTT conditions were used to reduce measurement variation.28 Study participants were asked to fast at least 8 h before the OGTT and to avoid unusual physical activity (sports) on the day before the test. Furthermore, they should not smoke prior to or during the OGTT. Glucose tolerance was not tested in cases of acute infections (fever) or any acute gastrointestinal problems, in particular, vomiting or diarrhoea. OGTT were not performed after 11:00 a.m. Tests were carried out by trained and quality-certified study nurses only. Newly diagnosed diabetes and IGT were defined according to the 1999 WHO criteria.29
Definitions of SES variables
Items related to SES were assessed in a structured health interview performed by trained investigators. Education was classified based on the highest level obtained: primary (Hauptschule, Volksschule), secondary (Mittlere Reife, Realschule) and tertiary (Abitur, Fachhochschulreife, Universität) education. Codes concerning occupations were extracted from an index proposed by Helmert and Shea30 for German studies, as this code provides a good method for grouping different occupations according to a social class hierachy. According to the self-reports, three groups were categorized that reflect job position. For retired persons, the most recent occupation was coded. Among persons without regular employment (e.g. housewives), the occupation of the spouse was used as a proxy. Income was based on the total household net income, weighted by the number of household members in different age groups (i.e. equivalent household income). Income was classified into five groups according to the median income in the study population (<50%, 50–100%, 101–150%, 151–200% and >200% of the median income).
Anthropometric measurements and behavioural variables
Body weight was measured in light clothing to the nearest 0.1 kg and height to the nearest 0.5 cm. Waist circumference was measured at the maximum abdominal girth to the nearest 0.1 cm. Blood pressure was measured in a sitting position three times at the right arm after 15 min rest using an automatic device (OMRON HEM 705-CP). Means of the second and third measurement were included in the analysis.
In the structured interview, medical history was obtained including health-care utilization. Subjects were also asked to report the frequency and average duration of regular moderate and vigorous physical activity during leisure time in winter and summer using four categories. Less than 1 h activity per week was defined as low physical activity. Alcohol intake was assessed for the previous workday and the previous weekend. Increased intake was defined as >40 g per day in men and >20 g per day in women. Current smoking was defined as at least one cigarette per day on a regular basis.
Laboratory measurements
Blood glucose was measured using a hexokinase method (Gluco-quant; Roche Diagnostics, Mannheim, Germany). High-density lipoprotein (HDL) cholesterol was assessed using the phosphotungstic acid method (Boehringer Mannheim). Triglycerides were measured with the Boehringer GPO-PAP assay.28
Statistical analysis
Analyses were carried out separately for men and women, accounting for sampling weights and clustering (Stata Statistical Software, release 7.0; StataCorp, College Station, TX, USA). Descriptive analyses were obtained for all variables and differences between men and women were assessed using Student's t-test or 
2-tests. Sex differences in SES indicators were evaluated using linear regression models including ordinal SES variables. Means [standard deviation (SD)] for normal distributed and geometric means (SD factor) for log-normal distributed continuous variables, or proportions for categorical variables, were calculated among the SES groups. Age-adjusted trends were evaluated using linear or logistic regression models. Prevalence of newly diagnosed diabetes and IGT in the various SES groups were calculated. Age-adjusted trend tests for diabetes and IGT were carried out by including ordinal variables for SES in logistic regression models. Finally, the associations of education, occupation and income with newly diagnosed diabetes or IGT were assessed using logistic regression models. SES indicators were included as dichotomous variables using the lowest class as reference (for income the lowest two classes). Age and fully adjusted models were fitted including potential risk factors. The level of significance was 5%.
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Characteristics of study participants
Demographic and behavioural characteristics, and risk factors among male and female survey participants are shown in table 1. Waist circumference, blood pressure and triglyceride concentrations were higher and HDL cholesterol was lower among men than women, indicating a more severe risk factor profile (P < 0.05). Low physical activity was found in >50% of both men and women (P
0.05). Current smoking and increased alcohol intake was more often reported in men, whereas no significant sex differences were observed for self-reported health-care utilization (hospitalizations and physician visits) (table 1).
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The distribution of SES indicators is shown in table 1. Significant sex differences were found for educational level, occupational status and income, which were all lower among women (P < 0.05). In both men and women, there was a skewed distribution of educational levels, with about 70% in the lowest group, as expected for this elderly population. In the age group aged 55–64 years, 39.8% of male and 32.6% of female survey participants were already retired.
After excluding all subjects with known diabetes, 10.6% of men and 7.5% of women had previously undiagnosed diabetes based on the OGTTs. Furthermore, the prevalence of IGT did not differ between men (18.5%) and women (17.3%).
SES and risk factors of type 2 diabetes
The distribution of various risk factors by SES are shown in table 2. In men, a significant inverse relation between body mass index (BMI) and education was found (P < 0.05), whereas no association was observed with waist circumference and physical activity (P > 0.05). Current smokers were more frequently found in the lowest educational category in men (P < 0.05). No significant relation with education was found for blood pressure, serum lipids and health-care use in men (data not shown).
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Occupational status yielded a significant inverse association with low physical activity in men (table 2). A similar relation was found with current smoking (both P < 0.05). Income also showed an inverse relationship with less physical activity in men (P < 0.05). Increased alcohol intake was most frequently reported in the highest income groups among male participants (P < 0.01). No significant SES differences were found for parental diabetes history in men (e.g. education: low, 20.4%; medium, 23.1%; high, 23.0% subjects with parental diabetes; P = 0.72).
In women, the associations of SES with body weight and physical activity were stronger than among men. A decrease of BMI, waist circumference and low physical activity with higher status was found for all three SES indicators (P < 0.05) (table 2). Using the 80th sex-specific percentiles for waist circumference among normal glucose-tolerant subjects as cut-off (men >109 cm; women >100 cm), the associations of SES indicators with abdominal adiposity were also stronger among women than men. Significant trends for abdominal obesity were found for all three SES indicators among women but not in men (P < 0.01). Current smoking also varied among the SES groups; however, there was no clear trend. Alcohol intake showed the highest prevalence in women with highest education (P < 0.05).
Whereas blood pressure was inversely related to education and occupation in women (P < 0.05), lipids did not significantly vary with SES indicators, except for HDL cholesterol and occupation (increase with higher status) (P < 0.05). Similar to men, no association of SES indicators with health-care utilization or parental diabetes history was found (all data not shown).
SES indicators and glucose tolerance groups
Prevalence of newly diagnosed diabetes and IGT according to socioeconomic indicators are shown in table 3. The relationship between occupation and newly diagnosed diabetes or IGT was inverse and graded in both sexes; however, this was only statistically significant for diabetes in women (P = 0.01). In both men and women, a borderline significance was found for occupation and IGT (P = 0.08).
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For education, no trends for newly diagnosed diabetes or IGT were found in either sex. Prevalence of newly diagnosed diabetes and IGT also varied within the income groups in men and women; however, no systematic variation could be found.
Multivariate associations of SES with glucose tolerance groups
In women, a significantly reduced risk of undiagnosed diabetes was found with higher occupational status, which was unchanged after adjusting for risk factors [odds ratio (OR) 0.5; 95% confidence interval (CI) 0.3–0.9]. Also, for income a borderline significance was found (adjusted OR 0.7; 95% CI 0.5–1.03). Education was not significantly associated with unknown diabetes in female participants, although the point estimate of the OR was well below 1.0.
In women, separate models for occupation were also fitted after excluding all participants without regular employments (e.g. housewives) (n = 87). The point estimates of the ORs were similar to the whole sample; however, they were no longer statistically significant owing to the lower sample size (data not shown).
In men, no significant associations of education, occupation or income with newly diagnosed diabetes were found in the multivariate models (table 4).
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With respect to IGT, higher occupational status yielded a significant inverse association with IGT in men, which persisted after adjusting for confounders (P < 0.05). Education and income were not related to the odds of having IGT in male participants (table 4).
In women, no significant associations of occupation or income with IGT were found, whereas there was increased risk for IGT with higher education in the multivariate model using primary education as baseline (OR 1.6; 95% CI 1.2–2.3).
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Discussion |
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In the KORA Survey 2000, a strong inverse association between SES, defined by occupation, and the odds of having undiagnosed diabetes was found in women aged 55–74 years. There was also an indication for an increased risk of unknown diabetes in women with lower income. In men, no significant relations between these SES indicators and undiagnosed diabetes were found. However, risk of IGT was increased in men with low SES (occupation) even after controlling for obesity, low physical activity and other risk factors.
Sex differences in the risk of known diabetes and SES have been reported previously.1,4 In the Third National Health and Nutrition Examination Survey, SES was significantly associated with type 2 diabetes in both African-American and white women, whereas no relationship was found for men.1 In the National Population Health Survey in Canada, low income and education remained significantly associated with self-reported diabetes after controlling for BMI and physical activity in women.4 In men, the associations were weaker and did not persist after controlling for risk factors.
The reasons for sex differences in the association of SES with type 2 diabetes are unclear. Unhealthy behaviour, unequal access to health care, nutritional factors, psychological stress, depression, or pre- and perinatal environmental factors have been proposed as possible mechanisms linking SES to diabetes.1,18 Lower social class in childhood was associated with increased insulin resistance in later life, the hallmark of type 2 diabetes.19,20 Low socioeconomic position in childhood was also related to increased prevalence of obesity in adulthood, even after adjusting for adult social class.19 Effect modification by sex in the association between SES and obesity was found in several studies, being stronger in women than in men.24 It is noteworthy, that in the present analysis, an inverse association of all three SES indicators with waist circumference or abdominal adiposity was found in women only. Abdominal adiposity is a central hallmark of the insulin resistance syndrome.25 Physical inactivity is another major behavioural risk factor of type 2 diabetes. Women with higher SES are more physically active than women with low SES, whereas this social gradient may be less pronounced in men.14,31
In line with previous investigations, health-care utilization was not related to SES and undiagnosed diabetes in the present study.1 However, only the uptake of health care services was assessed, and not what providers did if the system was accessed.21
Prevalence of IGT was inversely related to occupational status in men in the KORA survey. Furthermore, higher education was significantly associated with an increased risk of IGT in women. This was an unexpected finding, in particular because education was not significantly related to diabetes risk. In a previous study among Hong Kong Chinese, no significant relationship between SES, defined by education and occupation, and IGT was found.22 However, the study was based on a sample with high diabetes risk, mainly comprising women.23 IGT refers to an intermediate metabolic state between normal glucose tolerance and diabetes, and not all subjects with IGT will progress to manifest type 2 diabetes.23,29
Thus, the heterogeneity of persons with IGT most likely explains the different associations between SES and diabetes in the present study.
The KORA OGTT study included the age group 55–74 years because of their known increased risk of type 2 diabetes.28 There is little information on the extent of health inequalities related to SES in elderly populations. Some studies have suggested that health inequalities decrease with increasing age,32 but other studies have indicated that health inequalities are similar in all age groups.33 In Germany, one study suggested that the extent of health inequalities in cardiovascular disease, which is closely related to type 2 diabetes, is relatively small in the age group 60–69 years.34 Therefore, in the age-group included in the present study one would not expect as clear health inequalities as observed in younger age groups. Our results confirmed this expectation, as a mixed picture concerning the association with different SES variables was found. Special attention should be paid to the fact that different SES variables yielded different results. In the present study, health inequalities based on occupation were more pronounced than those based on income or education. In order to better disentangle the complex picture, it can be recommended that different SES variables should be used and compared in future studies.
Several limitations of this study need to be considered. Despite enormous efforts, the participation rate in the KORA Survey was only 62%, which may have introduced selection bias related to SES. Furthermore, it might be considered as drawback that subjects with known diabetes were not included. However, the selection of newly diagnosed type 2 diabetes allowed us to study the association with SES among incident cases. Subjects with known diabetes reflect determinants of development as well as duration of the disease. It is conceivable that in some patients with long-standing diabetes and severe disabling diabetic complications, poor health may result in low SES. Furthermore, residential area and housing tenure as aspects of SES were not included in the study because the study area is rather homogeneous in this respect. There are only small areas with markedly differing residential characteristics and only few participants would be expected to come from those areas.
In conclusion, undiagnosed diabetes was related to low SES in women. This association was most pronounced if SES is measured by occupational status. Known risk factors for type 2 diabetes may only partly explain this relation. In men, no significant associations between SES indicators and unknown diabetes were found. However, a significantly increased risk of IGT was found in men with low SES even after controlling for obesity, physical activity and other risk factors. The influence of SES on the development of type 2 diabetes needs to be further investigated.
Key points
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Acknowledgments |
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The authors are indebted to K. Papke (head of KORA Study Center) and B. Schwertner (survey organization) and their co-workers for organizing and conducting the data collection. We also thank all participants of the OGTT study. The OGTT study was partly funded by the German Federal Ministry of Health, the Ministry of School, Science and Research of the State of North-Rhine-Westfalia, and the Anna Wunderlich-Ernst Jühling Foundation (to W.R. and G.G.). The KORA Survey 2000 was financed by the GSF, which is funded by the German Federal Ministry of Education, Science, Research and Technology and the State of Bavaria.
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