These pages are best viewed with Netscape version 3.0 or higher or Internet Explorer version 3.0 or higher. When viewed with other browsers, some characters or attributes may not be rendered correctly.ORIGINAL ARTICLE Fiber Intake, Serum Cholesterol Levels, and Cardiovascular Disease in European Individuals With Type 1 Diabetes Monika Toeller, MD OBJECTIVE— A cross-sectional analysis of dietary fiber intake was performed in European type 1 diabetic patients enrolled in the EURODIAB IDDM Complications Study to explore its potential relationship to serum cholesterol levels and the prevalence of cardiovascular disease (CVD). RESEARCH DESIGN AND METHODS— Dietary intake was assessed by a standardized 3-day dietary record. For analysis of fiber intake (total, soluble, and insoluble) and its associations with CVD (past history or electrocardiogram abnormalities), complete data were available from 1,050 male and 1,012 female individuals. Relationships of fiber intakes to serum cholesterol levels (total, HDL, and LDL cholesterol) were examined in 926 men and 881 women with type 1 diabetes. RESULTS— Higher intakes of total fiber (g/day) were independently associated with significantly higher levels of HDL cholesterolin male (P = 0.01) and female individuals (P = 0.03). Fiber intakes of men with type 1 diabetes were also inversely related to ratios of total cholesterol to HDL cholesterol (P = 0.0001) and levels of LDL cholesterol (P = 0.0002). A protective effect of total fiber intake against CVD was observed for female subjects, where a significant trend was maintained after adjustment for potential confounders, including energy and saturated fat (P = 0.03 vs. P = 0.2 in men). Results were similar in separate analyses of soluble and insoluble fiber. CONCLUSIONS— The present study demonstrates that higher fiber intakes are independently related to beneficial alterations of the serum cholesterol pattern in men and to a lower risk for CVD in European insulin-dependent women. Beneficial effects can already be observed for fiber amounts within the range commonly consumed by outpatients with type 1 diabetes. Diabetes Care 22 (Suppl. 2):B21–B28, 1999 Long-term intervention studies in individuals with hyperlipidemia have demonstrated that fiber intakes of 30–60 g/day can effectively reduce cholesterol levels, namely LDL cholesterol (1–5). Some studies even reported a concomitant increase in HDL cholesterol (2,5). These effects of fiber intake are also highly relevant for the management of diabetes, as beneficial alterations of serum cholesterol are regarded as a main target for the prevention of cardiovascular disease (CVD) (6,7). In patients with type 1 diabetes, significantly lower levels of total cholesterol and LDL cholesterol have been found after consumption of diets providing 50–96 g fiber/day (8–12). However, these reductions in total and LDL cholesterol were often accompanied by decreases in HDL cholesterol, with no net improvement in the ratio of total cholesterol to HDL cholesterol (8,10,11,13). Moreover, general conclusions from these studies are hampered because the studies included only small numbers of subjects and because the fiber amounts employed exceeded by far the quantities commonly consumed by European individuals with type 1 diabetes (14). In large epidemiological studies conducted in the general population, fiber intakes were inversely related to risks for morbidity (15–19) or mortality (18–22) from CVD itself. However, despite the fact that diabetic patients have an increased risk of both morbidity and mortality due to CVD (23–25), possible benefits of fiber on CVD have not yet been investigated systematically in individuals with type 1 diabetes. In the present study, dietary fiber intakes commonly consumed by a large cohort of European outpatients with type 1 diabetes enrolled in the EURODIAB IDDM Complications Study were analyzed for possible relations to serum cholesterol levels as well as to the prevalence of CVD. RESEARCH DESIGN AND METHODS— The EURODIAB IDDM Complications Study is a cross-sectional, clinic-based study including 3,250 individuals with type 1 diabetes from 31 European centers. The study measured the prevalence of diabetic complications and examined established and putative risk factors associated with these complications. Details of the patient selection and the standardized methodology have previously been published (14,26–31). Each center selected a random sample of type 1 diabetic patients stratified by sex, age, and diabetes duration. The study conformed to the Declaration of Helsinki, and the study protocol was approved by local ethics committees in each center. Informed consent was given by all participants with type 1 diabetes. For the present study, data for soluble and insoluble fiber were appended to the previously used EURODIAB nutrient database (14,30). Thus, intakes of fiber (total fiber, soluble fiber, insoluble fiber), carbohydrate, fat (total fat, saturated fat, cholesterol), protein, alcohol, and energy were determined from the 3-day food records. Dietary records comprising 2 workdays and a Sunday were completed by individuals with type 1 diabetes according to instructions from their local dietitian. Thereafter, the records were coded by the dietitian using a centrally prepared EURODIAB food list and finally rechecked and computed at the Nutrition Co-ordinating Center in Düsseldorf. Presence of CVD was assessed by the clinical history of myocardial infarction, angina pectoris, stroke, or coronary artery bypass graft surgery and by 12-lead resting electrocardiograms suggestive of probable or possible ischemia as determined by Minnesota coding (27). For analysis, patients reporting any cardiovascular event were defined as aware of their CVD and those who had CVD determined by electrocardiogram only were considered to suffer unconsciously from CVD. Total cholesterol, HDL cholesterol, and triglycerides were determined using fasting serum and standard enzymatic methods (Guy's Hospital Medical School, London). LDL cholesterol levels were calculated using the Friedewald equation (32). HbA1c values were determined in London (The Royal London Hospital) using an enzyme immunoassay with a notably low normal range of 2.9–4.8%. Resting blood pressure was measured with a random zero sphygmomanometer. The mean of two readings to the nearest 2 mmHg was used for analysis. Information on physical activity and on whether persons were currently smoking was available from a questionnaire completed by all individuals. Statistical analysis The relationships between fiber intakes and serum cholesterol levels were analyzed by least-squares linear regression. Fiber intakes were included in the models either as continuous variables or as a series of dummy variables, where a separate variable was assigned for each level of total fiber intake (<10 g, 10–15 to >30 g). Mean serum cholesterol levels calculated for each category of fiber intake were adjusted for age, sex, total energy intake, saturated fat intake (% of energy), BMI, and vigorous exercise at least once a week. In models with HDL cholesterol, self-reported alcohol consumption (none, <20, >20 g/day) was also accounted for. For the analysis of the relation between fiber intake and serum cholesterol, patients taking lipid-lowering medication (n = 41) were excluded. In 8 of the 30 centers, nonfasting blood samples were collected, and 23 patients had fasting triglycerides levels exceeding 4.02 mmol/l (350 mg/dl). Thus, LDL cholesterol levels could only be calculated for a total of 1,807 individuals (926 men, 881 women); subsequent analyses of the relation between fiber intake and serum cholesterol levels are based on the results from these individuals. For analysis of the association between fiber consumption and the
prevalence of CVD, fiber intakes were expressed as quartiles. Trends over these quartiles
were examined univariately by variance analysis or the Cochran-Mantel-Haenszel All statistical analyses were carried out using the SAS program (33).
RESULTS Fiber intake and serum cholesterol levels
Figure 1 illustrates that total fiber intake (g/day) was related to HDL cholesterol levels. An increase of mean HDL cholesterol in higher categories of fiber intake could be observed for both male (Fig. 1A) and female (Fig. 1B) individuals with type 1 diabetes. In men, mean adjusted HDL cholesterol increased from 1.27 mmol/l (95% CI 1.17–1.38 mmol/l) in the lowest category to 1.43 mmol/l (95% CI 1.35–1.52 mmol/l) in the categories of men consuming >30 g fiber per day. The test for a linear relationship revealed a significant overall trend for men in the bivariate analysis and in the multivariate model (P = 0.004 and P = 0.01, respectively). For women, the association became significant after adjustment for potential confounders (P = 0.2 and P = 0.03, respectively). Adjusted mean HDL cholesterol in women with type 1 diabetes increased from 1.57 mmol/l (95% CI 1.47–1.67 mmol/l) in those consuming only <10 g fiber per day to 1.71 mmol/l (95% CI 1.56–1.86 mmol/l) in the highest category. The ratio of total cholesterol to HDL cholesterol was also significantly related to fiber intakes of men with type 1 diabetes, with the adjusted ratio falling from 4.6 (95% CI 4.2–5.1) in men with a fiber intake <10 g/day to a ratio of 3.5 (95% CI 3.1–3.8) in men whose fiber intake exceeded 30 g/day (test for trend: P = 0.0001). For women with type 1 diabetes, a decrease was observed, from a ratio of 3.8 (95% CI 3.4–4.2) in the lowest category of fiber intake (<10 g/day) to 3.3 (95% CI 2.8–3.9) in the highest category of fiber intake (>30 g/day); however, the overall trend was not significant (P = 0.2).
Figure 2 shows that a significant relationship between fiber intake and LDL cholesterol was found for male subjects (Fig. 2A), but not for female subjects (Fig. 2B). In men with type 1 diabetes, adjusted mean LDL cholesterol decreased from 3.5 mmol/l (95% CI 3.2–3.7 mmol/l) for individuals consuming <10 g of fiber/day to 2.9 mmol/l (95% CI 2.8–3.1 mmol/l) for those with a fiber intake of >30 g/day. Separate examination of soluble and insoluble fiber intakes for a relation to serum cholesterol levels yielded comparable results, with no substantial differences between the two fiber fractions. When analyses were repeated and adjusted for dietary cholesterol (mg/day) or total fat (% of energy) intake in place of saturated fat intake, comparable results were obtained (data not shown). Fiber intake and CVD
Potential confounders for CVD by quartiles of total fiber intake are given in Tables 2 and 3. Male and female patients with higher intakes of fiber consumed more total energy and less saturated fat. In addition, men in the upper quartiles of fiber intake tended to consume less alcohol, to be leaner and more physically active, and to smoke less. Women with higher fiber intakes were older and smoked less frequently, but they suffered more often from hypertension.
Figure 3 illustrates the sex-specific independent relation between the presence of CVD and total fiber intake. For women with type 1 diabetes, bivariate analysis yielded significant inverse associations of the presence of CVD with all three fiber fractions (total fiber, P = 0.01; soluble fiber, P = 0.01; and insoluble fiber, P = 0.01). After adjustment for potential confounders, the significant trends were attenuated but maintained for total fiber (P = 0.03) and insoluble fiber (P = 0.03), with total energy and saturated fat partially explaining the associations. In men with type 1 diabetes, fiber intakes were not related to the presence of CVD either in bivariate or in multivariate analysis. Stratified analysis according to the awareness of CVD revealed lower rates of CVD in women with higher total fiber intakes, both for women who knew they had CVD (test for trend: P = 0.05) and for those unaware of the disease (test for trend: P = 0.1). By contrast, a significant trend of the presence of CVD to increase with higher total fiber intakes was observed for men aware of their CVD (P = 0.01); for men unconscious of having CVD at the time of the study, no relation was found (P = 1.0). Compared with men without CVD, men with CVD had higher LDL cholesterol levels (3.6 [95% CI 3.4–3.9] vs. 3.2 [95% CI 3.1–3.2] mmol/l) and lower HDL cholesterol levels (1.34 [95% CI 1.25–1.43] vs. 1.39 [95% CI 1.37–1.41] mmol/l). Similar differences were observed between women with and without CVD (LDL cholesterol: 3.3 [95% CI 3.1–3.5] vs. 3.2 [95% CI 3.2–3.3] mmol/l; HDL cholesterol: 1.56 [95% CI 1.47–1.64] vs. 1.65 [95% CI 1.62–1.67] mmol/l). However, further adjustments for LDL or HDL cholesterol did not materially change the results (data not shown). When analyses were repeated while accounting for total fat (% of energy) or cholesterol intake (mg/day) in place of saturated fat, comparable results were obtained. CONCLUSIONS— This is the first epidemiological study to report an association between fiber intake and serum cholesterol levels for European individuals with type 1 diabetes. Our results demonstrate that fiber intakes of male type 1 subjects are significantly related to levels of HDL and LDL cholesterol and to the ratio of total cholesterol to HDL cholesterol. In female individuals with type 1 diabetes, fiber intakes were significantly associated with HDL cholesterol levels.These relations were observed independently of other nutritional factors, namely intakes of dietary fat. Some epidemiological studies in the general population have not found a significant independent beneficial effect of fiber intake on HDL cholesterol (34–37). However, the Framingham Nutrition Study recently reported a significant association for postmenopausal women (38), and the Multiple Risk Factor Intervention Trial found HDL cholesterol to be significantly related to men's insoluble fiber intake (39). In past years, HDL cholesterol has been recognized as an important "negative" CVD risk factor (7), and more recent epidemiological studies have also addressed the ratio of total cholesterol or LDL cholesterol to HDL cholesterol. In the present study, we observed an inverse association of fiber intake with the ratio of total cholesterol to HDL cholesterol. Similar findings have been reported from the latest follow-up of the Framingham Nutrition Study for postmenopausal women (38) and from the Multiple Risk Factor Intervention Trial in middle-aged men, where the proportion of LDL cholesterol to HDL cholesterol was significantly associated to intakes of total fiber, soluble fiber, and insoluble fiber (39). The present study also showed an independent association of fiber intake to LDL cholesterol, although this association was confined to male type 1 diabetic patients. For nondiabetic men, several epidemiological studies have found significant inverse associations between serum LDL cholesterol and fiber intake (36,39–41). Conversely, evidence for nondiabetic women is less convincing; some studies did not find a relation to fiber intake (36,40) and others reported only a weak association that disappeared after adjustment for potential confounders (35). Whether these differences are truly sex-specific or whether confounders particularly relevant for women, such as the use of estrogens, mask the relations has not yet been fully answered. Unfortunately, in this study, we do not have detailed information on estrogen use, either as hormonal replacement therapy in postmenopausal women or as oral contraceptive. However, the oral contraceptives used at the time of the study exert adverse effects mainly on serum triglyceride levels, and only to a smaller extent on levels of both HDL cholesterol and LDL cholesterol (42). Moreover,higher fiber intakes are also associated with decreases in estradiol and estrone plasma levels (43–45). Considering that estrogens promote a decrease of LDL cholesterol (7), it may be that the beneficial effect of fiber on LDL cholesterol is counteracted by the lowering effect of fiber on estrogen plasma concentrations. Despite the fact that in the present study influences of fiber intake on the presence of CVD were analyzed only cross-sectionally in a relatively young study cohort (mean age 33 years), we could demonstrate an independent protective effect of fiber intake for the presence of CVD in female type 1 diabetic patients, even after adjustment for other lifestyle factors characterizing a healthier lifestyle often associated with higher fiber intakes. A relation of fiber intake to the morbidity and mortality from CVD has been reported by several epidemiological follow-up studies in the general population. Although in some of these studies adjustment for energy intakes accounted for the observed relation (16,21,22), other large population-based longitudinal studies found inverse relations between fiber intake and CVD, independent of other nutritional factors (17–19,20). Women with type 1 diabetes experience a relative increase of their risk for CVD after diabetes onset, with the risk eventually comparable to that of type 1 men (24,27,46). Thus, it is of particular interest that women in this study benefited from the protective effect of fiber against CVD. At first sight,this finding does not appear in line with the weak associations seen between the fiber intake of women and their cholesterol levels. However, other studies have reported that the protection against coronary events associated with increased fiber intake is larger than the risk reduction expected from alterations of the serum cholesterol pattern (18–20). Moreover, in the present study, levels of LDL cholesterol or HDL cholesterol did not explain the association between fiber intake and presence of CVD. Thus, alternative mechanisms have to be assumed for the protective effects of fiber intake on CVD, e.g., concomitant increases in intakes of antioxidants (47,48), influences on hemostasis (49,50), or blood pressure (51). For the men with type 1 diabetes in this study, we could not show an effect of increased fiber intake on the risk for CVD. However, a cross-sectional analysis cannot clearly disentangle "real" associations from lifestyle modifications generated, e.g., by the diagnosis of CVD. Nevertheless, the trend of CVD prevalence to increase with higher intakes of fiber in male subjects aware of their CVD suggests that some of the men reporting a higher fiber consumption in this study had modified their nutritional behavior after disease diagnosis.In fact, the Scottish Heart Health Study also reported that specifically men aware of their CVD had apparently changed their dietary habits subsequent to disease diagnosis, whereas a similar effect was not observed for women (15). In conclusion, the present study demonstrates that higher fiber intake is independently related to beneficial alterations of the serum cholesterol pattern in men and to a lower risk for CVD in women with type 1 diabetes. These beneficial effects could already be shown for a cohort of European outpatients with type 1 diabetes with a mean fiber intake of only 17.4 g per day. Presumably, further increases of fiber intake will provide additional benefits, particularly for the large number of patients who consume less fiber than the 20–40 g fiber per day currently recommended for individuals with diabetes (52–54). Acknowledgments— This study was part of the EURODIAB Concerted Action Programme financially supported by the Commission of the European Community. Additional financial support was received from the research funds of the Nutrition Co-Ordinating Centre at the Diabetes Research Institute in Düsseldorf to analyze the nutritional data. The participation of the patients in the study is gratefully acknowledged. We thank all dietitians and nutritionists in the EURODIAB centers for their excellent cooperation. APPENDIX— EURODIAB Centers and Investigators: B. Karamanos, C. Tountas, A. Kofinis, K. Petrou, N. Katsilambros, and D. Roussi-Penessi, Hippokration Hospital, Athens, Greece; M. Cignarelli, R. Giorgino, M. L. De Geco, and I. Ramunni, Cattedra di Endocrinologia-Policlinico, Bari, Italy; C. Ionescu-Tirgoviste, R. Strachinariu, and A. Nicolau, Clinic of Diabetes, Nutrition and Metabolic Diseases, Bucharest, Rumania; G. Tamas, Z. Kerenyi, A. M. Ahmed, J. Toth, and P. Kempler, Tetenyi Teaching Hospital and Semmelweis University, Budapest, Hungary; S. Muntoni, M. Songini, M. Stabilini, M. Fossarello, and S. Pintus, Ospedale San Michele, Cagliari, Italy; B. Ferriss, C. C. Cronin, and M. Humphreys, Cork Regional Hospital, Ireland; M. Toeller, A. Klischan, T. Forst, F. A. Gries, and W. Schumacher, Diabetes-Forschungsinstitut, Universität Düsseldorf, Germany; R. Rottiers, H. Priem, and M. J. Deschoolmeester, University Hospital of Gent, Belgium; P. Ebeling, M. Sinisalo, and V. A. Koivisto, University Hospital of Helsinki, Finland; B. Idzior-Walus, B. Solnica, L. Szopinska-Ciba, and K. Solnica, University School of Medicine, Krakow, Poland; H. M. J. Krans, H. H. P. J. Lemkes, J. J. Jansen, and B. M. Elte-de Wever, University Hospital of Leiden, The Netherlands; J. Nunes-Correa, J. Boavida, R. Carvalho, M. J. Afonso, M. Monteiro, and R. David, Portuguese Diabetic Association, Lisbon, Portugal; E. Jepson and S. McHardy-Young, Central Middlesex Hospital, NW London, U.K.; J. H. Fuller, D. J. Betteridge, M. Milne, and T. Thompson, University College Hospital, NW London, U.K.; G. Michel, R. Wirion, S. Paquet, and H. Hornick, Centre Hospitalier, Luxembourg; A. J. M. Boulton, H. Ashe, D. J. S. Fernando, and J. Curwell, Manchester Royal Infirmary, U.K.; G. Pozza, G. Slaviero, G. Comi, B. Fattor, F. Bandello, and M. Marchi, Ospedale San Raffaele, Milan, Italy; H. Mehnert, A. Nuber, H. Janka, M. Nichting, and E. Standl, City Hospital Schwabing, Munich, Germany; G. Crepaldi and R. Nosadini, Istituto di Medicina Interna, University ofPadua, Italy; G. Cathelineau, B. Villatte Cathelineau, M. Jellal, N. Grodner, P. Gervais Feiss, and N. Baclet, Hospital Saint-Louis, Paris, France; F. Santeusanio, G. Rosi, M. R. M. Ventura, C. Cagini, and C. Marino, Instituto di Patologia Medica, Policlinico, Perugia, Italy; R. Navalesi, G. Penno, R. Miccoli, M. Nannipieri, S. Manfredi, and A. Bertolotto, Instituto di Clinica Medica II, Pisa, Italy; G. Ghirlanda, P. Cotroneo, A. Manto, C. Teodonio, A. Minnella, and G. Careddu, Universita Cattolica del Sacro Cuore, Rome, Italy; J. D. Ward, S. Tesfaye, C. Mody and C. Rudd, Royal Hallamshire Hospital, Sheffield, U.K.; G. M. Molinatti, F. Vitelli, M. Porta, G. F. Pagano, P. Estivi, R. Sivieri, Q. Carta, and G. Petraroli, Clinica Medica B, Patologia Medica, Ospedale Molinette, and Ospedale "Agnelli," Turin, Italy; N. Papazoglou, M. Goutzourela, and C. Manes, General Hospital of Thessaloniki, Greece; D. Ben Soussan, M.-C. Fallas, P. Fallas, C. Dhanaeus, and M. D. Bourgeois, Centre Hospitalier de Valenciennes, France; M. Muggeo, V. Cacciatori, F. Bellavere, P. Galante, M. L. Gemma, and P. Branzi, Cattedra di Malatties del Metabolismo, Verona, Italy; K. Irsigler, H. Abrahamian, C. Gurdet, B. Hornlein, C. Willinger, H. Strohner, and M. Just, Hospital Vienna Lainz, Austria; S. Walford, E.V. Wardle, S. Henio, and H. Cooke, New Cross Hospital, Wolverhampton, U.K.; and G. Roglic, Z. Resman, Z. Metelko, and Z. Skrabalo, Vuk Vrhovac Institute for Diabetes, Zagreb, Croatia. Steering Committee members: J. H. Fuller (London); H. Keen (London), Chairman; H. M. J. Krans (Leiden); R. Navalesi (Pisa); A.-K. Sjolie (Aarhus); J. M. Stephenson (London); M. Toeller (Düsseldorf); G.-C. Viberti (London); J. Ward (Sheffield). Data Co-Ordinating Centre: J. H. Fuller, University College London, Department of Epidemiology and Public Health, London. Nutrition Co-Ordinating Centre: M. Toeller, Diabetes Research Institute, Heinrich-Heine-University, Düsseldorf, Germany. Central Laboratories: G. John, The Royal London Hospital, and G.-C. Viberti, M. Mattock, A. Collins, A. Dredge, and R. 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Ser., no. 797) From the Clinical Department of the Diabetes Research Institute (M.T., A.E.B., G.H.) at the Heinrich-Heine-University, Düsseldorf, Germany; the Institute of Clinical Medicine, Endocrinology and Metabolic Diseases (G.d.P., F.G.), University of Bari, Italy; and the Department of Epidemiology and Public Health (J.H.F.), University College London Medical School, London, U.K. Address correspondence and reprint requests to Monika Toeller, MD, Clinical Department, Diabetes Research Institute at the Heinrich-Heine-University, Auf'm Hennekamp 65, 40225 Düsseldorf, Germany. Received for publication 27 May 1998 and accepted in revised form 20 August 1998. Abbreviations: CVD, cardiovascular disease. This article is based on a presentation at a satellite symposium of the 16th International Diabetes Federation Congress. The symposium and the publication of this article were made possible by educational grants from Hoechst Marion Roussel AG. Copyright © 1999 American Diabetes Association For Technical Issues contact webmaster@diabetes.org |
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test. Logistic regression was employed for calculation of crude and adjusted odds ratios.
For trend testing in the logistic models, fiber intakes (g/day) were fitted as continuous
variables. The key confounders considered were age, diabetes duration, sex, total energy
intake, saturated fat intake (% of energy), alcohol intake (no intake, <20 g,
>20 g/day), BMI, current smoking, physical activity (vigorous exercise at least once a
week), presence of hypertension (blood pressure >140/90 mmHg or antihypertensive
medication) and levels of HbA1c. All patients for whom these data were
available were included in the analysis so as to achieve the largest possible database.
Models are based on 2,062 individuals (1,050 men, 1,012 women) mainly because of missing
centrally measured HbA1c concentrations.
)in different categories of fiber intake (<10 to >30
g/day) for male (A) (n = 926) and female (B) (n = 881)
individuals with type 1 diabetes. Columns indicate percentage of subjects in each fiber
category. Mean HDL cholesterol levels with 95% CIs (vertical lines) are adjusted for age,
total energy intake, saturated fat intake (% of energy), BMI, vigorous exercise at least
once a week, and self-reported alcohol intake (none, <20 g, >20
g).
