Open Access
Open Peer Review

This article has Open Peer Review reports available.

How does Open Peer Review work?

The association of education with body mass index and waist circumference in the EPIC-PANACEA study

  • Silke Hermann1,
  • Sabine Rohrmann1, 37Email author,
  • Jakob Linseisen1, 2,
  • Anne M May3, 4,
  • Anton Kunst5,
  • Herve Besson3, 6,
  • Dora Romaguera7,
  • Noemie Travier8,
  • Maria-Jose Tormo9, 10, 11,
  • Esther Molina11, 12,
  • Miren Dorronsoro11, 13,
  • Aurelio Barricarte11, 14,
  • Laudina Rodríguez15,
  • Francesca L Crowe16,
  • Kay-Tee Khaw17,
  • Nicholas J Wareham6,
  • Petra GA van Boeckel4,
  • H Bas Bueno-de-Mesquita4,
  • Kim Overvad18, 19,
  • Marianne Uhre Jakobsen19,
  • Anne Tjønneland20,
  • Jytte Halkjær20,
  • Claudia Agnoli21,
  • Amalia Mattiello22,
  • Rosario Tumino23,
  • Giovanna Masala24,
  • Paolo Vineis25, 26,
  • Androniki Naska27,
  • Philippos Orfanos27,
  • Antonia Trichopoulou27, 28,
  • Rudolf Kaaks1,
  • Manuela M Bergmann29,
  • Annika Steffen29,
  • Bethany Van Guelpen30,
  • Ingegerd Johansson31,
  • Signe Borgquist32,
  • Jonas Manjer33,
  • Tonje Braaten34,
  • Guy Fagherazzi35,
  • Françoise Clavel-Chapelon35,
  • Traci Mouw7,
  • Teresa Norat7,
  • Elio Riboli7,
  • Sabina Rinaldi36,
  • Nadia Slimani36 and
  • Petra HM Peeters3
BMC Public Health201111:169

DOI: 10.1186/1471-2458-11-169

Received: 6 September 2010

Accepted: 17 March 2011

Published: 17 March 2011

Abstract

Background

To examine the association of education with body mass index (BMI) and waist circumference (WC) in the European Prospective Investigation into Cancer and Nutrition (EPIC).

Method

This study included 141,230 male and 336,637 female EPIC-participants, who were recruited between 1992 and 2000. Education, which was assessed by questionnaire, was classified into four categories; BMI and WC, measured by trained personnel in most participating centers, were modeled as continuous dependent variables. Associations were estimated using multilevel mixed effects linear regression models.

Results

Compared with the lowest education level, BMI and WC were significantly lower for all three higher education categories, which was consistent for all countries. Women with university degree had a 2.1 kg/m2 lower BMI compared with women with lowest education level. For men, a statistically significant, but less pronounced difference was observed (1.3 kg/m2). The association between WC and education level was also of greater magnitude for women: compared with the lowest education level, average WC of women was lower by 5.2 cm for women in the highest category. For men the difference was 2.9 cm.

Conclusion

In this European cohort, there is an inverse association between higher BMI as well as higher WC and lower education level. Public Health Programs that aim to reduce overweight and obesity should primarily focus on the lower educated population.

Keywords

socioeconomic status education BMI waist circumference cohort study EPIC

Background

Overweight and obesity are growing problems worldwide with a prevalence of overweight and obesity of 60% for European women and 70% for men in the age group of 45-59 years [1]. Being overweight or obese increases the risk of some types of cancer, cardiovascular disease, hypertension, diabetes mellitus type 2, gallstones, osteoarthritis, or sleep apnea [2]. In most Western countries, there is a clear association between socioeconomic status (SES) and the risk of becoming overweight or obese as pointed out by McLaren [3]. Data from NHANES 1999/2000 survey have shown a higher prevalence of obesity in low educated men and women compared with high educated subjects, although the difference between these groups decreased between the survey in the early 1970s and the 1999/2000 survey [4]. In the WHO MONICA project, years of schooling and BMI were also significantly inversely associated [5]. In contrast to the US results, MONICA results indicate an increase in the gap between obesity in less and better educated subjects in most of the participating centers. It is interesting to note that in both surveys a trend towards a higher education in the survey populations has been observed.

Although body mass index (BMI) is the most commonly used anthropometric measure of obesity, other measures such as waist circumference (WC) are increasingly being used. WC is of special interest since previous evaluations of the European Prospective Investigation into Cancer and Nutrition (EPIC) have shown that WC was stronger related to overall mortality than BMI [6]. EPIC-PANACEA (Physical Activity, Nutrition, Alcohol, Cessation of smoking, Eating out of home And obesity) offers the opportunity to evaluate the association between highest educational level attained and measurements of BMI and WC in a large European population.

Methods

Population and study design

EPIC is an ongoing multi-centre prospective cohort study consisting of 23 centres in 10 countries (Denmark, France, Germany, Greece, Italy, the Netherlands, Norway, Spain, Sweden and the United Kingdom). From 1992 to 2000, more than 500,000 individuals (in majority 35 to 70 years of age) were recruited from the population living in a defined geographical region. Recruitment procedures have been described in detail by Riboli et al. [7]. The cohort of France is based on female members of a health insurance plan for school employees; parts of the Italian and Spanish cohorts included members of local blood donors associations; the cohorts from Utrecht (The Netherlands) and Florence (Italy) recruited participants of breast cancer screening programs; and the Oxford cohort consisted of vegetarians, vegans and other health-conscious individuals. In France, Norway, Utrecht (The Netherlands) and Naples (Italy) only women were recruited [7]. Baseline information on education, occupation, medical history, tobacco smoking, physical activity and reproductive history were assessed using questionnaires and/or interviews. Usual diet was measured by country-specific assessment instruments. Seven countries adopted an extensive self-administered dietary questionnaire. In Greece, Spain and Ragusa a dietary questionnaire was administered by direct interview. A food frequency questionnaire and a seven-day record were adopted in the UK. In Malmö, Sweden, a quantitative questionnaire combined with a 7-day menu book and an interview was used [7]. Approval for this study was obtained from the ethical review boards of all participating institutions.

Of the total cohort of 519,931 apparently healthy subjects, we excluded subjects with missing information on dietary and non-dietary variables (n = 6,675), BMI (n = 4,011), or education (n = 20,170), subjects with an extreme ratio of energy intake to energy expenditure (n = 10,209), pregnant women (n = 623), and subjects with implausible anthropometric measurements (n = 376). The analytical cohort consisted of 141,230 men and 336,637 women.

Anthropometric measurements

In most EPIC centres height and weight were measured at recruitment following a standardized procedure and is described in detail elsewhere [8]. In France, Oxford and Norway, self-reported data were obtained from all individuals. For part of the Oxford (UK) cohort, for which measured data were not available, linear regression models were used to predict sex- and age-specific values from subjects with both measured and self-reported body measures [9, 10]. In each centre, WC was measured either at the narrowest torso circumference or midway between the lower ribs and the iliac crest. To reduce heterogeneity due to protocol differences in clothing worn during measurement, correction factors of - 1.5 kg for weight and - 2.0 cm for WC were adopted for subjects who were normally dressed and without shoes, while an adjustment for weight of - 1.0 kg was applied for subjects in light clothing [8]. While BMI information (measured or self-reported) was available for all subjects, WC measurements were only available for 73% of the subjects as waist circumference has not been measured in Norway, Umea (Sweden), and in the majority of the French cohort.

BMI was calculated as weight (kg) divided by height (m) squared. We used the following BMI categories: < 18.5 kg/m2, underweight; BMI ≥ 18.5 to < 25 kg/m2, normal weight; BMI ≥ 25 to < 30 kg/m2, overweight; BMI ≥ 30 kg/m2, obese.

Highest Level of Education

Educational level, based on highest school level reached (university, secondary, technical or professional, primary, or none), was used as a proxy for SES. This variable was categorized into: (1) primary school or less; (2) vocational secondary education; (3) other secondary education; and (4) university degree.

Covariates

Recruitment age, smoking, physical activity, alcohol consumption, total energy intake and marital status were taken into account as co-variables. Smoking status was categorized as current, former, never and missing. To adjust for the level of physical activity, a five-level validated variable (inactive, moderately inactive, moderately active, active, and missing) was created [11]. Information on alcohol consumption reflected the amount of alcohol consumed daily during the 12 months prior to recruitment. This information was summarized in a six-level variable for women (non consumers, 1-6, 7-18, 19-30, 31-60, > 60 g/day) and a seven-level variable for men (non consumers, 1-6, 7-18, 19-30, 31-60 g/day, 61-96, > 96 g/day). Total energy intake was computed from the dietary assessment instruments. Marital status was categorised as single/separated/widowed, living together/married and missing.

Statistical methods

The associations between BMI, WC and education were examined for the total EPIC cohort and by country. All analyses were carried out by sex. The association between education and BMI or WC across all countries was estimated using multilevel mixed linear models with random intercepts and coefficients both at the centre and country level. The analysis by countries was done depending on the number of study centres per country. For countries with only one centre (i.e., the Netherlands [men], France, Norway, and Greece), adjusted linear models were run. For countries with more than one study centre (i.e., Italy, Spain, the Netherlands [women], Sweden, Denmark, Germany, and United Kingdom,), adjusted mixed linear models with random intercept at centre level were used to assess the association between highest education level and BMI/WC.

In all models, BMI and WC were modelled as continuous variables. Education level was the independent variable and modelled using a categorical variable. Age at recruitment and total energy intake were entered in the models as continuous variables while physical activity, smoking, and alcohol consumption were entered in the models as categorical variables. Further adjusting for marital status did not change our results and was not included in the final models. Secondary analyses were performed by age group (age at recruitment </≥ 60 years), smoking status, categories of alcohol consumption (0-<6/≥6 g/day), as well as by BMI (</≥25 kg/m2) and WC (</≥88 cm in women; </≥102 cm in men [12]). All statistical analyses were performed with SAS software version 9.1 (SAS Institute, Cary, NC, USA).

Results

The distribution of educational levels varies widely in the EPIC cohort (Table 1). The percentage of men having only completed primary school ranged from 10.9% (Dutch cohorts) to 38.7% (Spanish centers); in women, the country with the lowest percentage of subjects that have only completed primary school was in the French cohort, which consists of female school employees (11.1%) and highest in the Spanish cohorts (41.8%). In the Italian cohorts, 14.4% of men had a university degree compared to 42.5% in the two German cohorts; in women, the lowest percentage of women with university degree was observed in the Spanish cohorts (10.0%) and the highest in the British cohorts (39.5%). Besides the Greek and the Spanish cohorts, only few study participants fell into the category with no formal educational degree. Therefore, we had combined the categories "no degree" and "primary school completed" into "primary school or less".
Table 1

Distribution of EPIC participants by sex, country, and highest level of education attained

  

Men

Women

  

Educational Level

Educational Level

  

1

2

3

4

Total

1

2

3

4

Total

France

n

--

--

--

--

--

7944

--

35437

25699

69080

 

%

--

--

--

--

--

11.5

--

51.3

37.2

 

Italy

n

2426

2130

7626

2041

14223

9270

3461

14317

4172

31220

 

%

17.1

15.0

53.6

14.4

 

29.7

11.1

45.9

13.4

 

Spain

n

9308

1952

1206

2232

14698

18651

1375

1390

2385

23801

 

%

63.3

13.3

8.2

15.2

 

78.4

5.8

5.8

10.0

 

United Kingdom

n

3214

6514

2514

7827

20069

5457

14471

7152

17699

44779

 

%

16

32.5

12.5

39.0

 

12.2

32.3

16.0

39.5

 

The Netherlands

n

1093

4136

2079

2681

9989

5213

9425

8797

5253

28688

 

%

10.9

41.4

20.8

26.8

 

18.2

32.9

30.7

18.3

 

Greece

n

5393

1962

1581

1718

10654

9557

1007

2891

1816

15271

 

%

50.6

18.4

14.8

16.1

 

62.6

6.6

18.9

11.9

 

Germany

n

5512

6137

1156

9446

22251

7017

12260

2316

7833

29426

 

%

24.8

27.6

5.20

42.5

 

23.9

41.7

7.9

26.6

 

Sweden

n

8460

4930

4790

4649

22829

10064

7715

4685

6982

29446

 

%

37.1

21.6

20.98

20.4

 

34.2

26.2

15.9

23.7

 

Denmark

n

9193

7769

2054

7501

26517

9128

13568

3455

2996

29147

 

%

34.7

29.3

7.8

28.3

 

31.3

46.6

11.9

10.3

 

Norway

n

--

--

--

--

--

8206

12800

10306

4467

35779

 

%

--

    

22.9

35.8

28.8

12.5

 

Total

n

44599

35530

23006

38095

141230

90507

76082

90746

79302

336637

1 = no formal degree or primary school completed ("primary school or less"); 2 = vocational secondary training; 3 = other secondary education; 4 = university

Baseline characteristics of the study participants are shown in Table 2. Subjects with a low educational level were oldest at time of recruitment, had the highest prevalence of overweight and obesity of all education categories, and reported the lowest level of physical activity. Men and women with a university degree were less often current smokers than participants who were less educated. Women with the lowest education also had the lowest alcohol consumption.
Table 2

Baseline Characteristics of EPIC participants by sex and highest level of education; 1992-2000

 

Men

Women

 

Primary school or less

Vocational secondary education

Other secondary education

University

Primary school or less

Vocational secondary education

Other secondary education

University

n (%)

44599 (31.6)

35530 (25.2)

23006 (16.3)

38095 (27.0)

90507 (26.9)

76082 (22.6)

90746 (27.0)

79302 (23.6)

 

Median (interquartile range)

Age at recruitment (years)

56.7 (50.6-61.8)

52.1 (45.5-58.5)

48.7 (40.4-56.0)

51.4 (43.5-57.7)

54.7 (48.7-60.9)

51.1 (44.4-56.7)

50.2 (44.5-56.1)

48.3 (42.9-54.3)

Total energy intake (kcal/day)

2381 (1954-2877)

2341 (1938-2806)

2439 (2008-2931)

2304 (1927-2730)

1823 (1498-2209)

1807 (1508-2157)

1958 (1620-2355)

1935 (1608-2311)

Alcohol consumption at baseline (g/d)

12.6 (3.0-32.6)

12.8 (4.2-29.4)

12.1 (3.7-28.1)

15.0 (6.1-30.9)

1.5 (0.0-7.3)

3.8 (1.0-10.6)

4.0 (0.7-11.9)

6.2 (1.6-13.8)

BMI (kg/m2)

27.2 (24.9-29.7)

26.1 (24.1-28.4)

25.7 (23.6-28.0)

25.4 (23.4-27.6)

26.3 (23.6-29.8)

24.3 (22.1-27.2)

23.3 (21.3-25.8)

22.7 (20.9-25.1)

WC (cm)

97.0 (91.0-104.0)

94.0 (87.5-100.0)

92.3 (86.3-99.0)

92.0 (86.0-98.0)

85.0 (77.0-93.0)

77.5 (71.2-85.3)

77.0 (71.0-84.0)

74.0 (69.0-80.8)

 

Percent

Prevalence of overweight (%)a

51.8

50.0

46.5

45.1

38.2

31.2

24.4

20.1

Prevalence of obesity (%)a

22.5

14.2

12.1

9.9

23.9

11.7

7.4

5.4

Smoking status

        

   Never

27.4

30.2

34.8

40.8

60.9

46.5

56.4

56.3

   Former

37.0

37.9

34.6

35.7

16.3

26.8

22.5

26.2

   Smoker

34.6

31.1

29.5

22.6

21.3

25.4

18.2

15.2

   Missing

1.0

0.8

1.1

0.9

1.5

1.2

3.0

2.4

Physical activity

        

   Inactive

20.5

14.8

14.9

16.3

33.6

13.9

18.0

14.1

   Moderately inactive

23.7

25.6

28.7

35.1

27.8

27.9

32.3

34.2

   Moderately active

22.4

22.0

19.4

23.0

14.4

18.5

22.3

27.0

   Active

24.8

26.8

19.7

18.4

10.7

17.9

11.3

14.5

   Missing

8.6

10.8

17.2

7.3

13.6

21.8

18.2

10.2

Marital status

        

   Single/divorced/separated/widowed

9.4

13.2

15.9

15.8

12.8

15.8

17.0

24.9

   Married/living together

48.3

58.4

65.8

58.3

54.5

61.5

74.8

66.5

   Missing

42.3

28.4

18.3

25.9

32.7

22.7

8.2

8.6

a overweight defined as BMI ≥ 25 and < 30, obesity defined as BMI ≥ 30

b does not add up to 100% due to missing information

Compared to women with lowest education, women with a university degree had a 2.12 kg/m2 lower BMI (Table 3). For men, result was similar although less pronounced (1.28 kg/m2). Crude results were similar compared with fully adjusted models. The difference between lowest and highest education group was larger in younger than in older women. The difference in BMI was also stronger in younger men, but less pronounced than in women. In women, the difference between highest and lowest educational group was stronger in never than in current smokers, but the confidence intervals were wide and overlapping. We observed strongly attenuated associations of education with BMI in non-obese subjects. In women, but not in men, the difference between highest and lowest education status was still statistically significant in non-obese subjects, but the difference was merely 0.5 BMI units.
Table 3

Associationa,b between level of education and BMI (kg/m2) in EPIC by sex and subgroups; EPIC participants interviewed between 1992 and 2000

 

Primary school or less

Vocational secondary training

Other secondary education

University

  

Estimate

95% CI

Estimate

95% Ci

Estimate

95% CI

BMI (kg/m 2 )

       

Women

       

Overall crude

ref.

-1.16

-2.46 to 0.14

-1.58

-2.69 to -0.47

-2.25

-3.39 to -1.10

Overall adjusteda

ref.

-0.98

-1.11 to -0.85

-1.44

-1.69 to -1.20

-2.12

-2.49 to -1.76

   Age > = 60

ref.

-0.84

-0.98 to -0.70

-1.25

-1.47 to -1.03

-1.56

-1.88 to -1.24

   Age < 60

ref.

-1.30

-1.56 to -1.04

-1.46

-1.72 to -1.20

-2.13

-2.48 to -1.78

Never smoker

ref.

-1.19

-3.45 to 1.08

-1.68

-3.70 to 0.35

-2.37

-4.42 to -0.32

Former smoker

ref.

-1.03

-2.16 to 0.10

-1.51

-2.56 to -0.45

-2.04

-3.08 to -0.99

Current smoker

ref.

-0.90

-1.52 to -0.29

-1.05

-1.65 to -0.45

-1.59

-2.23 to -0.95

   Alcohol intake 0- < 6 g/day

ref.

-1.10

-2.40 to 0.20

-1.54

-2.67 to -0.41

-2.23

-3.38 to -1.08

   Alcohol intake ≥ 6 g/day

ref.

-1.05

-2.14 to 0.04

-1.42

-2.35 to -0.50

-1.97

-2.91 to -1.03

BMI < 25 kg/m2

ref.

-0.15

-0.65 to 0.35

-0.27

-0.72 to 0.19

-0.47

-0.92 to -0.02

BMI ≥ 25 kg/m2

ref.

-0.57

-1.16 to 0.01

-0.76

-1.25 to -0.27

-1.08

-1.64 to -0.53

Men

       

Overall crude

ref.

-0.56

-1.68 to 0.56

-0.81

-1.91 to 0.29

-1.28

-2.45 to -0.10

Overall adj.

ref.

-0.52

-0.61 to -0.44

-0.84

-1.00 to -0.69

-1.28

-1.50 to -1.07

   Age > = 60

ref.

-0.61

-0.79 to -0.44

-0.70

-0.90 to -0.49

-0.97

-1.16 to -0.77

   Age < 60

ref.

-0.55

-0.68 to -0.43

-0.84

-1.01 to -0.67

-1.36

-1.55 to -1.18

Never smoker

ref.

-0.66

-1.27 to -0.06

-0.95

-1.59 to -0.31

-1.52

-2.23 to -0.82

Former smoker

ref.

-0.63

-0.99 to -0.27

-0.83

-1.24 to -0.42

-1.28

-1.80 to -0.75

Current smoker

ref.

-0.50

-1.67 to 0.67

-0.85

-2.03 to 0.33

-1.14

-2.34 to 0.05

   Alcohol intake 0- < 6 g/day

ref.

-0.67

-1.83 to 0.49

-0.89

-2.06 to 0.28

-1.42

-2.68 to -0.15

   Alcohol intake ≥ 6 g/day

ref.

-0.56

-1.16 to 0.04

-0.87

-1.46 to -0.28

-1.33

-2.02 to -0.64

BMI < 25 kg/m2

ref.

-0.01

-0.16 to 0.15

-0.02

-0.20 to 0.15

-0.04

-0.24 to 0.15

BMI ≥ 25 kg/m2

ref.

-0.52

-0.79 to -0.24

-0.62

-0.88 to -0.37

-0.95

-1.25 to -0.66

aadjusted for recruitment age, smoking, physical activity, alcohol consumption, total energy intake (when applicable)

bthe association between education and BMI or WC across all countries was estimated using multilevel mixed linear models with random intercepts and coefficients both at the centre and country level.

The direction of the overall association between BMI and education was consistent in all countries, although the strength of the association differed between countries. In women the association was weakest in the French cohort and strongest in the Greek cohort (Figure 1). In men, the weakest association was observed in the British centers, while the association was most pronounced in the Italian centers (Figure 2). For all countries, but men of the Greek and Danish cohorts there was a clear trend between level of education and BMI; however, in all countries, BMI was significantly lower for all three higher education categories compared with the lowest education level (data not shown).
https://static-content.springer.com/image/art%3A10.1186%2F1471-2458-11-169/MediaObjects/12889_2010_Article_2909_Fig1_HTML.jpg
Figure 1

Difference (mean and 95% CI) in BMI (in kg/m 2 ) between highest and lowest educational level in women; EPIC participants interviewed between 1992 and 2000. The dotted vertical line indicates the overall mean difference between highest and lowest educational level.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2458-11-169/MediaObjects/12889_2010_Article_2909_Fig2_HTML.jpg
Figure 2

Difference (mean and 95% CI) in BMI (in kg/m 2 ) between highest and lowest educational level in men; EPIC participants interviewed between 1992 and 2000. The dotted vertical line indicates the overall mean difference between highest and lowest educational level.

The association between WC and education level was stronger for women than for men: compared with the lowest education level, the average waist circumference was statistically significantly lower by 5.20 cm for female participants in the highest category (Table 4). For men the respective difference was 2.94 cm. Crude associations were similar to the fully adjusted models. Age stratification revealed a stronger difference in WC with education in elderly men compared to younger men. However, for women the difference was larger in the younger than in the older age group. As seen for BMI, the difference between highest and lowest educational group was stronger in never than in current smokers, but again with wide and overlapping confidence intervals. The observed differences were similar between non- or occasional consumers of alcoholic beverages and regular consumers (≥6 g ethanol/day). Even among women with a waist circumference < 88 cm, the difference between highest and lowest educated women was statistically significant, but not among men with normal waist (< 102 cm). When adding BMI to the statistical model, all associations for WC were attenuated and lost statistical significance (data not shown).
Table 4

Associationa,b between level of education and waist circumference (cm) in EPIC by sex and subgroups; EPIC participants interviewed between 1992 and 2000

 

Primary school or less

Vocational secondary education

Other secondary education

University

  

Estimate

95% CI

Estimate

95% Ci

Estimate

95% CI

Waist (cm)

       

Women

       

Overall crude

ref.

-3.23

-5.72 to -0.74

-3.98

-6.10 to -1.87

-5.43

-7.76 to -3.10

Overall adj.

ref.

-2.62

-2.94 to -2.30

-3.71

-4.32 to -3.10

-5.20

-6.10 to -4.30

   Age > = 60

ref.

-2.06

-2.54 to -1.58

-3.02

-3.49 to -2.56

-3.83

-4.74 to -2.91

   Age < 60

ref.

-3.39

-3.99 to -2.80

-4.09

-4.57 to -3.62

-5.47

-6.19 to -4.76

Never smoker

ref.

-3.66

-5.84 to -1.48

-4.44

-6.38 to -2.50

-5.85

-7.98 to -3.72

Former smoker

ref.

-2.94

-4.96 to -0.91

-3.73

-5.77 to -1.70

-5.06

-7.05 to -3.07

Current smoker

ref.

-2.69

-3.85 to -1.54

-2.88

-4.04 to -1.72

-4.11

-5.29 to -2.92

   Alcohol intake 0- < 6 g/day

ref.

-3.21

-5.59 to -0.83

-3.95

-6.02 to -1.89

-5.41

-7.73 to -3.09

   Alcohol intake ≥ 6 g/day

ref.

-3.37

-5.07 to -1.68

-4.02

-5.68 to -2.37

-5.19

-6.84 to -3.54

waist circumf. < 88 cm

ref.

-1.28

-2.57 to 0.01

-1.65

-2.91 to -0.40

-2.25

-3.51 to -0.98

waist circumf. ≥ 88 cm

ref.

-0.85

-1.47 to -0.23

-1.31

-1.70 to -0.91

-1.63

-2.32 to -0.94

Men

       

Overall crude

ref.

-1.49

-3.28 to 0.30

-1.75

-3.58 to 0.07

-2.84

-4.90 to -0.78

Overall adj.

ref.

-1.25

-1.50 to -1.01

-1.97

-2.41 to -1.54

-2.94

-3.55 to -2.33

   Age > = 60

ref.

-1.44

-1.95 to -0.93

-1.53

-2.07 to -.99

-2.15

-2.70 to -1.61

   Age < 60

ref.

-1.39

-1.71 to -1.08

-1.96

-2.39 to -1.53

-1.96

-3.63 to -2.67

Never smoker

ref.

-1.93

-3.64 to -0.22

-2.29

-4.03 to -0.55

-3.70

-5.60 to -1.80

Former smoker

ref.

-1.51

-3.17 to 0.14

-1.92

-3.71 to -0.14

-3.06

-4.99 to -1.12

Current smoker

ref.

-1.33

-4.66 to 2.01

-2.08

-5.48 to 1.32

-2.51

-5.88 to 0.86

   Alcohol intake 0- < 6 g/day

ref.

-1.67

-4.95 to 1.61

-2.05

-5.50 to 1.40

-3.26

-6.78 to 0.26

   Alcohol intake ≥ 6 g/day

ref.

-1.53

-3.26 to 0.21

-2.15

-3.88 to -0.42

-3.14

-5.07 to -1.22

Waist circumf. < 102 cm

ref.

-0.40

-1.61 to 0.82

-0.76

-2.10 to 0.57

-1.29

-2.67 to 0.09

Waist circumf. ≥ 102 cm

ref.

-0.60

-0.98 to -0.22

-0.54

-0.99 to -0.10

-1.03

-1.40 to -0.66

aadjusted for recruitment age, smoking, physical activity, alcohol consumption, total energy intake (when applicable)

bthe association between education and BMI or WC across all countries was estimated using multilevel mixed linear models with random intercepts and coefficients both at the centre and country level

These associations were observed in most countries, but the magnitude of the effect differed between countries. In females, the association was weakest in the British centers and strongest in women of the Greek cohort; no statistically significant difference was observed in French women (Figure 3). In almost all centers besides France, women with secondary school or technical/professional school also had significant lower waist circumference compared to women with low education. For men, the relation was smallest in the Danish cohorts and strongest in the Dutch centers (Figure 4). Men of the Greek and the Swedish cohorts had a non-significant difference in waist circumference in participants with secondary school and technical/professional school; for all other centers, the difference was statistically significant (data not shown).
https://static-content.springer.com/image/art%3A10.1186%2F1471-2458-11-169/MediaObjects/12889_2010_Article_2909_Fig3_HTML.jpg
Figure 3

Difference (mean and 95% CI) in waist circumference (in cm) between highest and lowest educational level in women; EPIC participants interviewed between 1992 and 2000. The dotted vertical line indicates the overall mean difference between highest and lowest educational level.

https://static-content.springer.com/image/art%3A10.1186%2F1471-2458-11-169/MediaObjects/12889_2010_Article_2909_Fig4_HTML.jpg
Figure 4

Difference (mean and 95% CI) in waist circumference (in cm) between highest and lowest educational level in men; EPIC participants interviewed between 1992 and 2000. The dotted vertical line indicates the overall mean difference between highest and lowest educational level.

Discussion

WC is a measure of central adiposity, while BMI is generally considered as an indicator of overall obesity. In this European cohort, we observed that higher educated participants had lower BMI and as well as smaller WC. However, when adjusting WC for BMI, the association of education with WC was strongly attenuated, indicating that BMI is a good indicator of the association between education and obesity.

This inverse association between BMI and educational level is in line with results in other studies [2, 3, 1315], some also showing a stronger association for women than for men [3, 5, 16, 17]. However, the reason for this difference is still mostly unclear. Differences between SES categories in physical activity and energy intake might explain part of the association between SES and BMI [18], but this is not observed in our and other studies [19]. Furthermore, it could not be shown that SES status affects either total energy intake or macronutrients composition of the diet [20]. Similarly, in EPIC total energy intake did not differ strongly between the education categories (see Table 2). Another explanation is that underreporting might be more common in less educated subjects. Individuals with a higher BMI as well as those who want to reduce weight tend to underreport dietary intake to a greater degree than individuals with lower BMI [2123]. This behaviour seems to be more common among women than among men in EPIC [24]. Since 74% of the subjects in the lowest education category are either overweight or obese, the impact of dietary underreporting may be more meaningful among less educated people. The observed inverse SES gradients in BMI and WC are, thus, likely underestimated. Furthermore, it can be speculated that foods with a high energy density and an unhealthy image are underreported. Energy expenditure is a further important factor that influences BMI. Subjects in the lowest education level stated to be inactive most frequently (22.4% of men and 38.9% of females). It has also been shown that individuals who overestimated energy expenditure on the physical activity records had a significantly higher BMI and percentage of body fat compared with those that accurately estimated their energy expenditure [25, 26].

Overall, we observed a difference in BMI of 2.12 kg/m2 in women and of 1.28 kg/m2 in men when comparing highest with lowest educational level. Although Molarius et al. [5, 27] did not estimate an overall difference in the MONICA surveys, our results are comparable with the MONICA results in range. It is interesting to note that the association between education and BMI was smallest in women from the Scandinavian centers as well as the UK cohort and the French. However, for France this could be explained by the relative homogenous SES level at study intake, because only teachers and other school employees were recruited. So, although at younger age the educational level might have differed, later on inequalities in SES disappeared. The association was strongest in Greece, but associations in the Spanish and Italian cohorts were more comparable to associations in centers from Middle Europe. Recently, Roskam et al. [27] showed that educational inequalities in overweight and obesity were largest in Mediterranean women, whereas they were largest in French, German, Belgian, and Czech women in the MONICA surveys [5]. For men, the inequalities are in general smaller and no clear geographical pattern emerge for Southern, Central, and Northern Europe [5, 27]. In our analysis, it has to be taken into account, that although most cohorts were recruited from the general population, the cohorts are in the majority not representative of a country. Furthermore, as some cohorts have been recruited from specific subgroups of the population such as blood donors comparisons between the cohorts should be interpreted with caution.

Our study includes a large sample size and participants from ten European countries. However, for some centers, i.e., France, Oxford, and Norway, only self-reported information was available. Assuming an underreporting of weight and WC in these centers that is stronger in less than better educated individuals, this would cause a weaker association between BMI and WC and SES compared with other centers. This is what we indeed observed (Figures 1, 2, 3 and 4), although we still observed statistically significant relations between BMI and education in these centers. Differences in measurement of waist circumference between centers might also partly explain differences in the association between waist circumference and education between the centers. The EPIC participants were recruited over a time period of eight years (from 1992 to 2000). Changes in the prevalence of obesity and changes in the structure of the educational system (i.e., a trend towards a higher education in the general population) might lead to a small cohort effect, such that the association between SES and BMI could be different between subjects that have been recruited at the beginning of this period and subjects that have been recruited towards the end. Our data was too limited to study this.

Education was used in our analysis as an indicator of SES. Low educational levels may influence obesity-related behaviour such as diet and physical activity, which may be caused by lack of knowledge [28]. Compared to occupation and income, education is stable throughout life and reflects childhood conditions. However, stability can be a limitation because it does not take social advancements and status later in life into account [29]. In addition, SES of the spouse may be important, too. Neglecting this may result in an error that is probably more severe in older women, who adapted the SES of their partners after marriage. This may also explain the stronger effect seen in younger subjects (< 60 years of age). However, adjusting for marital status did not change our study results. Further variables to better capture a subject's SES such as household income have not consistently been assessed in all EPIC centers. The fact that the educational systems are diverse in the various European countries may lead to further misclassification. However, the lowest (primary school or less) as well as the highest educational level (university degree) should be rather comparable for all countries. Also, efforts have been made to correct for misclassification by comparing highest school level with years of schooling.

Conclusion

In all European EPIC cohorts, there was an inverse association seen between BMI as well as WC and education level. Our results confirm previous literature on SES and BMI; as well add new information for the association between WC and level of education.

Public Health Programs that aim to reduce overweight and obesity should primarily focus on the lower educated population, such that these programs are better targeted to the addressed population group.

Declarations

Acknowledgements

The work described in this paper was carried out with support of the European Commission: Grant no DG Sanco, project number: 2005328.

The work was further financially supported by the European Commission: Public Health and Consumer Protection Directorate 1993-2004; Research Directorate-General 2005-."; Ligue contre le Cancer, Societé 3M, Mutuelle Générale de l'Education Nationale, Institut National de la Santé et de la Recherche Médicale (INSERM) (France); German Cancer Aid, German Cancer Research Center, Federal Ministry of Education and Research (Germany); Danish Cancer Society (Denmark); Health Research Fund (FIS) of the Spanish Ministry of Health, The participating regional governments and institutions (Spain); Cancer Research UK, Medical Research Council, Stroke Association, British Heart Foundation, Department of Health, Food Standards Agency, the Wellcome Trust (United Kingdom); Greek Ministry of Health and Social Solidarity, Hellenic Health Foundation and Stavros Niarchos Foundation (Greece); Italian Association for Research on Cancer, National Research Council (Italy); Dutch Ministry of Public Health, Welfare and Sports, Dutch Ministry of Health, Dutch Prevention Funds, LK Research Funds, Dutch ZON (Zorg Onderzoek Nederland), World Cancer Research Fund (WCRF) (the Netherlands); Swedish Cancer Society, Swedish Scientific Council, Regional Government of Skane (Sweden); Norwegian Cancer Society (Norway).

Authors’ Affiliations

(1)
Division of Cancer Epidemiology, German Cancer Research Centre
(2)
Institute of Epidemiology, Helmholtz Centre Munich
(3)
Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht
(4)
National Institute for Public Health and the Environment (RIVM)
(5)
Academic Medical Centre (AMC), University of Amsterdam
(6)
Medical Research Council, Epidemiology Unit, Institute of Metabolic Science
(7)
Department of Epidemiology & Public Health, Imperial College London
(8)
Unit of Nutrition, Environment and Cancer, Catalan Institute of Oncology, IDIBELL
(9)
Epidemiology Service, Murcia Health Council
(10)
Preventive Medicine and Public Health Unit, Murcia Medical School
(11)
CIBER Epidemiología y Salud Pública (CIBERESP)
(12)
Andalusian School of Public Health
(13)
Public Health Department of Gipuzkoa
(14)
Public Health Institute of Navarra
(15)
Public Health and Participation Directorate, Health and Health Care Services Council
(16)
Cancer Epidemiology Unit, University of Oxford
(17)
Department of Public Health and Primary Care, University of Cambridge
(18)
Department of Cardiology, Aalborg Hospital, Aarhus University Hospital
(19)
Department of Clinical Epidemiology, Aarhus University Hospital
(20)
Danish Cancer Society, Institute of Cancer Epidemiology
(21)
Nutritional Epidemiology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori
(22)
Department of Clinical and Experimental Medicine - Federico II University
(23)
Cancer Registry and Histopathology Unit, Department of Oncology, "Civile - M.P.Arezzo" Hospital
(24)
Molecular and Nutritional Epidemiology Unit, Cancer Research and Prevention Institute (ISPO)
(25)
ISI Foundation
(26)
Environmental Epidemiology, Imperial College London
(27)
Department of Hygiene and Epidemiology, University of Athens Medical School
(28)
Hellenic Health Foundation
(29)
German Institute of Human Nutrition Potsdam-Rehbrücke
(30)
Department of Medical Biosciences, Pathology, Umeå University
(31)
Department of Odontology, Umeå University
(32)
Department of Oncology, Lund University Hospital
(33)
Department of Surgery, Malmö University Hospital
(34)
Institute of Community Medicine, University of Tromsø
(35)
Inserm ERI20 and Paris South University, Institut Gustave-Roussy
(36)
International Agency for Research on Cancer
(37)
Insitute of Social and Preventive Medicine, University of Zurich

References

  1. James PT: Obesity: The worldwide epidemic. Clin Dermatol. 2004, 22 (4): 276-280. 10.1016/j.clindermatol.2004.01.010.View ArticlePubMedGoogle Scholar
  2. Wyatt SB, Winters KP, Dubbert PM: Overweight and obesity: prevalence, consequences, and causes of a growing public health problem. Am J Med Sci. 2006, 331 (4): 166-174. 10.1097/00000441-200604000-00002.View ArticlePubMedGoogle Scholar
  3. McLaren L: Socioeconomic Status and Obesity. Epidemiol Rev. 2007, 29 (1): 29-48. 10.1093/epirev/mxm001.View ArticlePubMedGoogle Scholar
  4. Zhang Q, Wang Y: Trends in the Association between Obesity and Socioeconomic Status in U.S. Adults: 1971 to 2000. Obesity Res. 2004, 12 (10): 1622-1632. 10.1038/oby.2004.202.View ArticleGoogle Scholar
  5. Molarius A, Seidell JC, Sans S, Tuomilehto J, Kuulasmaa K: Educational level, relative body weight, and changes in their association over 10 years: an international perspective from the WHO MONICA Project. Am J Public Health. 2000, 90 (8): 1260-1268. 10.2105/AJPH.90.8.1260.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Pischon T, Boeing H, Hoffmann K, Bergmann M, Schulze MB, Overvad K, van der Schouw YT, Spencer E, Moons KGM, Tjonneland A, et al: General and Abdominal Adiposity and Risk of Death in Europe. N Engl J Med. 2008, 359 (20): 2105-2120. 10.1056/NEJMoa0801891.View ArticlePubMedGoogle Scholar
  7. Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondiere UR, Hemon B, Casagrande C, Vignat J, et al: European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002, 5 (6B): 1113-1124. 10.1079/PHN2002394.View ArticlePubMedGoogle Scholar
  8. Haftenberger M, Lahmann PH, Panico S, Gonzalez CA, Seidell JC, Boeing H, Giurdanella MC, Krogh V, Bueno-de-Mesquita HB, Peeters PH, et al: Overweight, obesity and fat distribution in 50- to 64-year-old participants in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr. 2002, 5 (6B): 1147-1162. 10.1079/PHN2002396.View ArticlePubMedGoogle Scholar
  9. Spencer EA, Appleby PN, Davey GK, Key TJ: Validity of self-reported height and weight in 4808 EPIC-Oxford participants. Public Health Nutr. 2002, 5 (4): 561-565. 10.1079/PHN2001322.View ArticlePubMedGoogle Scholar
  10. Spencer EA, Roddam AW, Key TJ: Accuracy of self-reported waist and hip measurements in 4492 EPIC-Oxford participants. Public Health Nutr. 2004, 7 (6): 723-727. 10.1079/PHN2004600.View ArticlePubMedGoogle Scholar
  11. Wareham NJ, Jakes RW, Rennie KL, Schuit J, Mitchell J, Hennings S, Day NE: Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr. 2003, 6 (4): 407-413. 10.1079/PHN2002439.View ArticlePubMedGoogle Scholar
  12. WHO: Obesity: preventing and managing the global epidemic. Report on a WHO consultation. 2000Google Scholar
  13. Borodulin K, Mäkinen T, Fogelholm M, Lahti-Koski M, Prättälä R: Trends and socioeconomic differences in overweight among physically active and inactive Finns in 1978-2002. Prev Med. 2007, 45 (2-3): 157-162. 10.1016/j.ypmed.2007.02.007.View ArticlePubMedGoogle Scholar
  14. Hajian-Tilaki KO, Heidari B: Prevalence of obesity, central obesity and the associated factors in urban population aged 20-70 years, in the north of Iran: a population-based study and regression approach. Obes Rev. 2007, 8 (1): 3-10. 10.1111/j.1467-789X.2006.00235.x.View ArticlePubMedGoogle Scholar
  15. Aranceta J, Pérez-Rodrigo C, Serra-Majem L, Bellido D, de la Torre ML, Formiguera X, Moreno B: Prevention of overweight and obesity: a Spanish approach. Public Health Nutr. 2007, 10 (10A): 1187-1193. 10.1017/S1368980007000699.View ArticlePubMedGoogle Scholar
  16. Sabanayagam C, Shankar A, Wong TY, Saw SM, Foster PJ: Socioeconomic status and overweight/obesity in an adult Chinese population in Singapore. J Epidemiol. 2007, 17 (5): 161-168. 10.2188/jea.17.161.View ArticlePubMedGoogle Scholar
  17. Sánchez-Vaznaugh EV, Kawachi I, Subramanian SV, Sánchez BN, Acevedo-Garcia D: Do socioeconomic gradients in body mass index vary by race/ethnicity, gender, and birthplace?. Am J Epidemiol. 2009, 169 (9): 1102-1112.View ArticlePubMedGoogle Scholar
  18. Manios Y, Panagiotakos DB, Pitsavos C, Polychronopoulos E, Stefanadis C: Implication of socio-economic status on the prevalence of overweight and obesity in Greek adults: the ATTICA study. Health Policy. 2005, 74 (2): 224-232. 10.1016/j.healthpol.2005.01.014.View ArticlePubMedGoogle Scholar
  19. Drewnowski A, Specter SE: Poverty and obesity: the role of energy density and energy costs. Am J Clin Nutr. 2004, 79 (1): 6-16.PubMedGoogle Scholar
  20. Darmon N, Drewnowski A: Does social class predict diet quality?. Am J Clin Nutr. 2008, 87 (5): 1107-1117.PubMedGoogle Scholar
  21. Johansson G, Wikman A, Ahren AM, Hallmans G, Johansson I: Underreporting of energy intake in repeated 24-hour recalls related to gender, age, weight status, day of interview, educational level, reported food intake, smoking habits and area of living. Public Health Nutr. 2001, 4 (4): 919-927. 10.1079/PHN2001124.View ArticlePubMedGoogle Scholar
  22. Johansson L, Solvoll K, Bjørneboe GE, Drevon CA: Under- and overreporting of energy intake related to weight status and lifestyle in a nationwide sample. Am J Clin Nutr. 1998, 68 (2): 266-274.PubMedGoogle Scholar
  23. Braam LA, Ocke MC, Bueno-de-Mesquita HB, Seidell JC: Determinants of obesity-related underreporting of energy intake. Am J Epidemiol. 1998, 147 (11): 1081-1086.View ArticlePubMedGoogle Scholar
  24. Ferrari P, Slimani N, Ciampi A, Trichopoulou A, Naska A, Lauria C, Veglia F, Bueno-de-Mesquita HB, Ocke MC, Brustad M, et al: Evaluation of under- and overreporting of energy intake in the 24-hour diet recalls in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr. 2002, 5 (6B): 1329-1345. 10.1079/PHN2002409.View ArticlePubMedGoogle Scholar
  25. Buchowski MS, Townsend KM, Chen KY, Acra SA, Sun M: Energy expenditure determined by self-reported physical activity is related to body fatness. Obes Res. 1999, 7 (1): 23-33.View ArticlePubMedGoogle Scholar
  26. Irwin ML, Ainsworth BE, Conway JM: Estimation of energy expenditure from physical activity measures: determinants of accuracy. Obes Res. 2001, 9 (9): 517-525. 10.1038/oby.2001.68.View ArticlePubMedGoogle Scholar
  27. Roskam A-JR, Kunst AE, Van Oyen H, Demarest S, Klumbiene J, Regidor E, Helmert U, Jusot F, Dzurova D, Mackenbach JP, et al: Comparative appraisal of educational inequalities in overweight and obesity among adults in 19 European countries. Int J Epidemiol. 2009, dyp329-Google Scholar
  28. Ball K, Crawford D: Socioeconomic status and weight change in adults: a review. Soc Sci Med. 2005, 60: 1987-2010. 10.1016/j.socscimed.2004.08.056.View ArticlePubMedGoogle Scholar
  29. Regidor E: Measures of health inequalities: part 2. J Epidemiol Community Health. 2004, 58 (11): 900-903. 10.1136/jech.2004.023036.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Pre-publication history

    1. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2458/11/169/prepub

Copyright

© Hermann et al; licensee BioMed Central Ltd. 2011

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Advertisement