Dietary Intake of Total, Animal, and Vegetable Protein and Risk of Type 2 Diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-NL Study

Ivonne Sluijs; Joline W.J. Beulens; Daphne L. van der A; Annemieke M.W. Spijkerman; Diederick E. Grobbee; Yvonne T. van der Schouw

doi:10.2337/dc09-1321

Original Research

Dietary Intake of Total, Animal, and Vegetable Protein and Risk of Type 2 Diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-NL Study

Ivonne Sluijs, MSC¹,
Joline W.J. Beulens, PHD¹,²,
Daphne L. van der A, PHD³,
Annemieke M.W. Spijkerman, PHD²,
Diederick E. Grobbee, MD, PHD¹ and
Yvonne T. van der Schouw, PHD¹

¹Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, the Netherlands;
²Center for Prevention and Health Services Research, National Institute for Public Health and the Environment, Bilthoven, the Netherlands;
³Center for Nutrition and Health, National Institute for Public Health and the Environment, Bilthoven, the Netherlands.

Corresponding author: Ivonne Sluijs, i.sluijs-2{at}umcutrecht.nl.

Diabetes Care 2010 Jan; 33(1): 43-48. https://doi.org/10.2337/dc09-1321

Article Figures & Tables

Tables

Table 1

Baseline characteristics of the study population, according to quartiles of daily nutritional total protein intake

	Quartile 1 (low)	Quartile 2	Quartile 3	Quartile 4 (high)
Participants	9,523	9,524	9,524	9,523
Male sex	2,643 (27.8)	2,685 (28.2)	2,450 (25.7)	1,962 (20.6)
Age (years)	48 ± 12	48 ± 12	50 ± 12	51 ± 11
Energy intake (kcal/day)	2,036 ± 645	2,106 ± 618	2,078 ± 602	1,998 ± 622
Animal protein intake (g/day)	35.2 ± 7.0	44.5 ± 5.2	51.3 ± 5.2	62.9 ± 8.3
Vegetable protein intake (g/day)	27.0 ± 5.5	27.6 ± 4.8	27.6 ± 4.8	26.9 ± 4.7
Saturated fat intake (g/day)	31.2 ± 6.2	32.5 ± 5.6	33.0 ± 5.6	33.4 ± 5.9
Polyunsaturated fat intake (g/day)	15.3 ± 4.3	15.3 ± 3.8	14.9 ± 3.7	14.2 ± 3.6
Monounsaturated fat intake (g/day)	29.2 ± 5.5	29.7 ± 5.0	29.6 ± 5.0	29.2 ± 5.2
Cholesterol intake (mg/day)	190.0 ± 53.0	210.4 ± 51.1	223.4 ± 53.5	245.3 ± 64.2
Carbohydrate intake (g/day)	231.5 ± 34.3	223.7 ± 29.0	219.3 ± 28.2	213.6 ± 28.8
Glycemic load intake (g/day)	120.8 ± 24.7	114.7 ± 20.1	110.8 ± 18.9	106.0 ± 18.3
Fiber intake (g/day)	22.1 ± 5.2	23.2 ± 4.6	23.8 ± 4.6	24.2 ± 4.7
Vitamin C intake (mg/day)	101.4 ± 49.7	106.6 ± 43.1	111.6 ± 42.6	118.0 ± 44.0
Vitamin E intake (mg/day)	12.9 ± 3.6	12.5 ± 3.2	12.1 ± 3.0	11.5 ± 3.0
Magnesium intake (mg/day)	304.9 ± 46.2	327.2 ± 41.7	343.9 ± 40.9	365.9 ± 43.3
Iron intake (mg/day)	10.8 ± 1.6	11.3 ± 1.5	11.7 ± 1.6	12.1 ± 1.7
Heme iron intake (mg/day)	1.6 ± 0.7	1.9 ± 0.7	2.1 ± 0.7	2.5 ± 0.9
Alcohol intake (g/day)	15.8 ± 24.4	11.0 ± 15.9	9.7 ± 13.9	8.0 ± 12.6
BMI (kg/m²)	24.7 ± 3.7	25.3 ± 3.7	25.8 ± 3.9	26.7 ± 4.3
Waist circumference (cm)	83.1 ± 11.2	84.6 ± 11.2	85.5 ± 11.2	87.1 ± 11.7
Current smoker	3,655 (38.4)	3,014 (31.7)	2,541 (26.8)	2,420 (25.5)
Physically inactive*	3,983 (41.8)	3,609 (37.9)	3,482 (36.6)	3,413 (35.9)
Higher education	1,993 (20.9)	2,104 (22.1)	2,030 (21.3)	1,703 (17.9)
Parental history of diabetes	1,559 (16.4)	1,615 (17.0)	1,767 (18.5)	1,922 (20.2)
Systolic blood pressure (mmHg)	124.3 ± 18.6	125.3 ± 18.8	126.6 ± 18.7	127.8 ± 19.0
Diastolic blood pressure (mmHg)	77.2 ± 10.6	77.5 ± 10.5	78.0 ± 10.6	78.4 ± 10.7
Hypertension	3,108 (32.6)	3,307 (34.7)	3,491 (36.7)	3,762 (39.5)

Data are n (%) or means ± SD.
↵*Inactive according to Cambridge physical activity index.

Table 2

Univariable and adjusted HRs (95% CI) for the association between intake of protein, in quartiles and per 10 g, and incident type 2 diabetes

	Quartile 1 (low)	Quartile 2	Quartile 3	Quartile 4 (high)	P_trend	Per 10 g
Total protein
Cases/at risk (n)	153/9,523	185/9,524	249/9,524	331/9,523
Quartile median total protein (g/day)	64	72	79	88
Univariable	1	1.20 (0.97–1.49)	1.63 (1.33–1.99)*	2.15 (1.77–2.60)*	<0.001	1.36 (1.28–1.44)*
Model 1†: age and sex	1	1.17 (0.94–1.45)	1.50 (1.23–1.84)*	1.85 (1.53–1.25)*	<0.001	1.28 (1.22–1.36)*
Model 2‡: model 1 + dietary intake	1	1.24 (0.99–1.54)	1.65 (1.32–2.07)*	2.16 (1.69–2.76)*	<0.001	1.45 (1.34–1.56)*
Model 3§: model 2 + diabetes risk factors	1	1.16 (0.92–1.45)	1.45 (1.15–1.83)*	1.67 (1.29–2.16)*	<0.001	1.33 (1.22–1.45)*
Model 4‖: model 3 + waist and BMI	1	1.03 (0.82–1.29)	1.20 (0.95–1.51)	1.18 (0.91–1.53)	0.15	1.16 (1.06–1.26)¶
Animal protein
Cases/at risk (n)	155/9,523	182/9,524	243/9,524	338/9,523
Quartile median animal protein (g/day)	35	44	52	62
Univariable	1	1.16 (0.94–1.44)	1.56 (1.28–1.91)*	2.18 (1.80–2.63)*	<0.001	1.32 (1.25–1.39)*
Model 1†: age and sex	1	1.08 (0.87–1.33)	1.35 (1.10–1.65)¶	1.73 (1.43–2.10)*	<0.001	1.24 (1.17–1.30)*
Model 2‡: model 1 + dietary intake	1	1.17 (0.94–1.46)	1.54 (1.23–1.92)*	2.09 (1.64–2.67)*	<0.001	1.40 (1.30–1.51)*
Model 3§: model 2 + diabetes risk factors	1	1.09 (0.87–1.36)	1.31 (1.05–1.65)¶	1.58 (1.23–2.04)*	<0.001	1.28 (1.18–1.39)*
Model 4‖: model 3 + waist and BMI	1	0.99 (0.79–1.23)	1.11 (0.89–1.40)	1.14 (0.88–1.47)	0.22	1.13 (1.04–1.22)¶
Vegetable protein
Cases/at risk (n)	245/9,524	228/9,524	235/9,523	210/9,523
Quartile median vegetable protein (g/day)	22	26	29	33
Univariable	1	0.92 (0.76–1.10)	0.95 (0.79–1.13)	0.84 (0.70–1.01)	0.10	0.87 (0.76–0.99)¶
Model 1†: age and sex	1	0.94 (0.79–1.13)	1.02 (0.85–1.22)	1.02 (0.85–1.23)	0.64	1.01 (0.88–1.15)
Model 2‡: model 1 + dietary intake	1	0.89 (0.73–1.08)	0.96 (0.77–1.19)	0.91 (0.70–1.19)	0.63	0.85 (0.69–1.06)
Model 3§: model 2 + diabetes risk factors	1	0.95 (0.78–1.16)	1.03 (0.83–1.27)	1.05 (0.80–1.37)	0.63	0.97 (0.78–1.20)
Model 4‖: model 3 + waist and BMI	1	0.99 (0.82–1.21)	1.11 (0.89–1.38)	1.15 (0.88–1.50)	0.23	1.04 (0.83–1.29)

Data are HRs (95% CI).
↵*Significant at P < 0.001 level.
↵†Model 1: Corrected for sex (male or female) and age at recruitment (continuous).
↵‡Model 2: model 1 + energy-adjusted intake of saturated fat, monounsaturated fat, polyunsaturated fat, cholesterol, vitamin E, magnesium, fiber, and glycemic load (continuous).
↵§Model 3: model 2 + energy-adjusted alcohol consumption (<11, 11–25, 26–50, or >50 g/day), physical activity (not active, moderately inactive, moderately active, or active), mean systolic and diastolic blood pressure (continuous), education level (high, middle, or low), and parental history of diabetes (no, one parent, or both parents).
↵‖Model 4: model 3 + BMI (<20, 20–25 [reference group], 25–30, or >30 kg/m²), and waist circumference (continuous).
↵¶Significant at P < 0.05 level.

Table 3

Multivariable HRs (95% CI) for the association between the consumption of 5% energy from protein at the expense of 5% energy from fat or carbohydrates while keeping total energy intake constant and incident type 2 diabetes

	Model 3*	Model 4†
Total protein
Substitution protein for fat	1.72 (1.41–2.12)‡	1.31 (1.06–1.61)§
Substitution protein for carbohydrates	1.91 (1.52–2.40)‡	1.28 (1.01–1.61)§
Animal protein
Substitution protein for fat	1.51 (1.26–1.82)‡	1.19 (0.99–1.44)
Substitution protein for carbohydrates	1.72 (1.39–2.12)‡	1.20 (0.97–1.49)
Vegetable protein
Substitution protein for fat	1.13 (0.67–1.92)	1.32 (0.82–2.13)
Substitution protein for carbohydrates	0.97 (0.57–1.65)	1.17 (0.73–1.89)

Data are HRs (95% CI).
↵*Model 3: corrected for sex (male or female), age at recruitment (continuous), energy-adjusted intake of cholesterol, vitamin E, magnesium, fiber, and glycemic load (continuous), total energy intake (continuous), energy densities of fat, carbohydrates, and alcohol (per 5 energy %), physical activity (not active, moderately inactive, moderately active, or active), mean systolic and diastolic blood pressure (continuous), education level (high, middle, or low), and parental history of diabetes (no, one parent, or both parents).
↵†Model 4: model 3 + BMI (<20, 20–25 [reference group], 25–30, or >30 kg/m²) and waist circumference (continuous).
↵‡Significant at P < 0.001 level.
↵§Significant at P < 0.05 level.