Dietary fibre: influence on body weight, glycemic control and plasma cholesterol profile
Fibra dietética: influencia sobre el peso corporal, el control glicémico y el perfil del colesterol plasmático
N. Babio1,2, R. Balanza1,2, J. Basulto1, M. Bulló1,2 and J. Salas-Salvadó1,2
1Human Nutrition Unit. Department de Bioquímica i Biotecnologia. Facultat de Medicina i Ciències de la Salut. Hospital Universitari de Sant Joan. IISPV. Universitat Rovira i Virgili.
2CIBER Fisiopatología de la Obesidad y Nutrición CB06/03. Instituto de Salud Carlos III. Madrid. Spain.
ABSTRACT
There have been several studies on the effects of dietary fibre on the metabolism. Epidemiologic studies have consistently reported an inverse relationship between dietary fibre and type 2 diabetes mellitus or cardiovascular mortality. This review focuses on observational and experimental studies that examine the effect of different types and sources of dietary fibre on body weight, glucose metabolism and lipid profile.
From the available evidence, we conclude that clinical studies consistently show that the intake of viscous dietary fibre decreases the low density lipoprotein cholesterol and postprandial glucose levels, and induces short term satiety. However, few clinical trials have demonstrated that the intake of dietary fibre has a positive effect on the control of diabetes and body weight.
Key words: Dietary fibre. Body weight. Overweight. Obesity. Diabetes. Cholesterol.
RESUMEN
Existen diversos estudios que han evaluado el efecto del consumo de fibra dietética sobre el metabolismo. Diversos estudios epidemiológicos observaron una relación inversa entre la fibra dietética y la diabetes mellitas tipo 2 o la mortalidad cardiovascular. Esta revisión se basa sobre estudios observacionales y experimentales que han valorado los efectos de diferentes tipos y fuentes de fibra dietética sobre el peso corporal, el metabolismo de la glucosa y el perfil lipídico.
De la evidencia disponible, concluimos que los estudios clínicos consistentemente muestran que la ingesta de alimentos fuentes de fibra viscosa disminuye el colesterol de las lipoproteínas de baja densidad y los niveles de glucosa postprandial e induce la saciedad a corto plazo. Sin embargo, pocos ensayos clínicos han demostrado un efecto positivo sobre el control de la diabetes y el peso corporal.
Palabras clave: Fibra dietética. Peso corporal. Sobrepeso. Obesidad. Diabetes. Colesterol.
Introduction
Dietary fibre is a complex of non-digestible carbohydrates and lignin that are intrinsic and intact in plants and are resistant to digestion and absorption in the small intestine. Dietary fibre promotes beneficial physiological effects such as laxation, reduction in blood cholesterol and postprandial blood glucose modulation. Traditionally dietary fibre has been classified on the basis of its solubility in water (soluble or insoluble). However, the National Academy of Sciences Panel for the definition of dietary fibre recommended that the terms soluble and insoluble should be gradually replaced by terms referring to the specific beneficial physiological effects associated with the fibre: viscosity and fermentability1.
Dietary fibre is one of the most studied dietary components associated with a good cardiovascular health. Three decades ago it was suggested that a diet rich in non-refined carbohydrates and fibre is associated with a lower prevalence of chronic diseases,2,3 and the role of dietary fibre in human health and bodily mechanisms continues to be a subject of discussion within the scientific community.
Several longitudinal observational studies have shown a significant inverse relationship between fibre intake and cardiovascular and total mortality.4-8 A combined analysis of 10 prospective cohort studies conducted in the USA and Europe showed a 25% decrease in the risk of coronary disease for each 10 gram increase in fibre intake, after adjusting for several dietary and cardiovascular confounding factors.9 However, other studies suggest that cardiovascular benefits are, to a great extent, a direct consequence of eating whole-grain bread, green-leafy vegetables, fruit and vegetables, more than dietary fibre itself.10,11 Recently, Streppel et al.12 also observed that coronary heart disease mortality and all-cause mortality were reduced by 17% and 9% respectively for every additional 10 g of dietary fibre per day, with no clear associations for different types of dietary fibre.
Epidemiologic studies show that cereals, which are especially rich in insoluble fibre, protect the body from cardiovascular diseases and mortality. However, in clinical studies, only soluble viscous fibre has been demonstrated to have metabolic advantages. This paradox can be explained by the fact that food rich in fibre contains other phytochemical compounds that have been demonstrated to modulate inflammation, oxidation, insulin resistance and cholesterol metabolism. Likewise, it is possible that the effects attributed to fibre intake may instead be an indicator of lifestyle and of a healthy dietary pattern.
This review has focused on observational and experimental studies that have examined the effects of different types and sources (natural and synthetic) of dietary fibre on body weight, glucose metabolism, lipid profile and the prevention of cardiovascular diseases. Controversial issues, as well as limitations and clinical applications, are also discussed.
Fibre and body weight
Proposed mechanism of action
]]> There are several epidemiological studies suggesting an association between fibre intake and obesity or coronary heart disease. However, whether these associations are due to dietary fibre intake alone or to other possible dietary confounders is still a matter of some controversy. Dietary fibre can modulate body weight by various mechanisms. Fibre-rich foods usually have lower energy content, which contributes to a decrease into the energy density of the diet.13 Foods rich in fibre need to be chewed longer, leading to an increase in the time needed to eat the food and in the feeling of satiety. The fibres which make up viscous solutions also delay the passage of food from the stomach to duodenum and contribute to an increase in satiety and a decrease in energy consumption.14 In the intestine, the incorporation of fibre may complicate the union between digestive enzymes and their substrate, thus slowing down the absorption of nutrients.13 It is also important to note that the effects of dietary fibre consumption on body weight may be related to different gut hormones which regulate satiety, energy intake and/or pancreatic functions.15.Observational and epidemiological studies
Observational studies show that the obesity is less frequent in developing countries where there is high fibre consumption. In contrast, in recent decades the increased prevalence of obesity in developed countries has been accompanied by a decrease in the consumption of fibre and complex carbohydrates.16-19 In addition, it has been reported that vegetarian populations have a low risk of being overweight and obese, which suggests that dietary fibre consumption could play an important role in the prevention and development of obesity.20
A cross-cultural study of 16 cohorts in seven countries show that the BMI and subscapular skin fold thickness were inversely associated with total dietary fibre intake, suggesting that a reduced intake of fibre was an important determinant of body fat stores.18 A cross-sectional study (see table I) also showed that total soluble fibre intake was negatively associated with the energy intake and total body fat content.16 Alfieri et al.21 assessed the total fibre intake by means of 3-day food records in 3 population groups (one normal weight group, with a BMI between 20 and 27.0 kg/m2; one moderately obese group, with a BMI between 27.1 and 40 g/m2; and one severely obese group, with a BMI > 40.0 kg/m2). These authors showed that fibre intake was significantly higher in the normal weight group and was inversely associated with BMI after adjusting for several potential confounders (sex, age, education level and income). Recently, new research conducted as part of the PREDIMED study has also shown a significant inverse relationship between total dietary fibre consumption and body mass index or abdominal circumference.22
Prospective epidemiologic studies also support the relationship between the high consumption of fibre and a lower increase in weight.23-25 The CARDIA (The Coronary Artery Risk Development in Young Adults) study, a multicenter population-based cohort study carried out over 10 years, examined 2909 young individuals to determine the relationship between total dietary fibre intake and plasma insulin concentrations, weight and other cardiovascular diseases risk factors. After adjusting for BMI and multiple dietary (total energy, fat, alcohol intake) and potential non-dietary confounders (gender, education, physical activity, basal body weight, tobacco use), the study reported an inverse association between total fibre intake, plasma insulin concentrations and body weight gain23 (see table I) suggesting that fibre may play an important role in the prevention of insulin resistance and obesity. Individuals consuming higher amounts of fibre have a lower weight gain compared to those consuming lower amounts, independently of the level of total fat consumed. However, it has yet to be established whether body weight gain can be modulated by fibre intake or whether such observations are a consequence of a reverse causation bias or other uncontrolled factors. Controlled trials analyzing the effects of fibre on body weight change are required. Likewise, Liu et al.,24 in 2003 showed in the Nurses Health Study cohort that women in the highest quintile of dietary fibre intake had 49% lower risk of major weight gain than did women in the highest quintile. However, it is important to emphasize that these findings may reflect a healthy dietary pattern rather than fibre intake per se.
Experimental and clinical studies
Epidemiological data and mechanistic studies support the contention that fibre has beneficial effects on body weight regulation; however, there has been inconsistent data from randomized controlled clinical trials that have evaluated how body weight is affected by supplementing Fibre in the diet.26-29 In a systematic review, Howarth et al.19 analyzed several clinical trials conducted in small and heterogeneous population samples over relatively short periods of time (from 1 to 12 months). The findings were that the intake of 12 g fibre/day resulted in a decrease of 10% in energy intake and a body weight loss of 1.9 kg over 3.8 months.19 These authors indicated that this effect on body weight loss was greater in obese subjects.
The literature contains several reports of the effect of fibre supplements on body weight.19,29 However, only a few of the randomized placebo-controlled clinical trials used body weight (see table II) as the primary variable in the analysis.13 In addition, long-term (≥ 4 months) trials are rare30-33 and have only been conducted in small samples of heterogeneous populations (healthy controls, obese or diabetic patients) while using different types and doses of fibre.19
One of the best-studied fibre supplements in terms of its effects on body weight is guar gum. A meta-analysis of the randomized placebo controlled trials identified 34 guar gum trials of which only 11 could be analysed29 and only 2 were for a period > 14 weeks.30,33 The metaanalysis concluded that guar gum is not efficacious in reducing body weight and that it is frequently associated with gastrointestinal complaints such as flatulence, diarrhea, abdominal pain, and cramps.29
Other types of fibre supplements have been studied, also with inconclusive results with respect to weight control.34-36 Among these fibres, Plantago ovata and glucomannan are the most important. A large-scale study performed with ispaghula husk showed no significant short-term (3 weeks) differences in loss of body weight when comparing ispaghula, bran and control groups.34 Also, Rodriguez-Morán and coworkers27 analyzed Plantago psyllium to determine the lipid- and glucose-lowering efficacy of this type of fibre. They found that administering 5 g of Plantago psyllium had no significant short-term effects (6 weeks) on body weight in type II diabetic patients.27 In contrast, several studies have demonstrated that glucomannan supplements have a significant effect on appetite and body weight. However, only some of these studies were randomized placebo-controlled trials, and all were shortterm and performed in small study populations.35,37-39
Recently, we evaluated the effect of a mixed fibre supplement on body-weight loss, satiety, tolerability, lipid profile and glucose metabolism in a large sample of overweight or obese patients.40 We studied 166 overweight or obese patients in a parallel, double-blind, placebo-controlled clinical trial. These patients were randomized to receive a mixed fibre dose (Plantago ovata husk and glucomannan) or a placebo twice or 3 times a day in the context of a calorie restricted diet for a period of 16 weeks. Weight-loss tended to be higher for both fibre supplements (-4.52 ± 0.56 and -4.60 ± 0.55 kg) than for the placebo (-3.79 ± 0.58); however, the differences in changes between groups were not statistically significant.40
To conclude, there is sufficient evidence that body weight can be controlled by a high intake of fibre in the context of a diet that is high in fruit, vegetables, nuts, legumes, and whole grains. However, fibre supplementation cannot be systematically recommended for weight control because long-term adherence to a fibre supplemented diet is poor in adults41 and because there is still controversy surrounding the effects of fibre supplements on body weight.
Fibre and glycemic control
Proposed mechanism of action
Slavin and coworkers42 have shown that viscous soluble fibre plays an important role in controlling postprandial glycemic and insulin responses because of its effect on gastric emptying and macronutrient absorption from the gut.42 Surprisingly, the most prospective studies have found that insoluble fibre but not soluble fibre is inversely related to the incidence of type 2 diabetes mellitus (T2DM).43-47 To date, the physiopathology mechanisms that explain the beneficial effects of insoluble fibre have still not been clearly delimited.
Observational and epidemiological studies
]]> The results of prospective cohort studies (table III) were homogenous and consistently show that the risk for T2DM decreased between 21% and 82% (see fig. 1) across quintiles or quartiles (mean intake of 16 g/day to 302 g/day) of whole grain intake45,46,48-50 and between 21% and 30% (see fig. 2) across quintiles (mean intake of 2.3 g/day to 7.5 g/day) of total cereal fibre intake.43-47,51,52 This association was observed in both women and men and was statistically significant in all but one of the studies.46 However, it is important to emphasize that no analysis was carried out to determine whether this association differs according to the type of grain consumed or to determine the extent to which the structure of the grain or its constituents such as magnesium or vitamin E may explain its protective effect.
All the studies reviewed have analyzed large cohorts from 4316 to 91,249 participants from 6 to 12 years of follow-up. However, because all of these studies were performed in American individuals (except for that of Montonen et al.46 which was conducted in Finland), the generalizability of these findings is uncertain. Furthermore, the evidence from the prospective cohort studies is considered too weak to establish a definitive conclusion regarding the preventive effect of whole grain or cereal fibre consumption on the development of T2DM.
Experimental and clinical studies
Several randomized controlled trials (table IV) have been performed to determine the effect of dietary fibre from natural food on insulin sensitivity;53,54 blood glucose control;55-57 and hypoglycemic episodes55 or HbA1c levels.55,57,58 However, all of them were short term studies.
]]> Several studies conducted during the last decade regarding the effect of dietary fibre on insulin sensitivity provide controversial results. In a randomized cross-over study, Pereira and co-workers used a euglycemic-hyperinsulinemic clamp test to measure insulin sensitivity in 11 obese hyperinsulinaemic participants. Their results showed that a whole grain diet led to a postprandial improvement in insulin sensitivity when compared to a refined grain diet.53 Likewise, Weicker and co-workers54 used the same method to measure insulin sensitivity in overweight and obese women and found that this increased after 3 days of a diet containing bread enriched with insoluble fibre compared to another diet containing white bread. Giacco and co-workers55 carried out a 6-months randomized parallel study comparing a diet containing 50 g/d of soluble fibre with a diet containing only 15 g/d of fibre. They found an improvement in the daily blood glucose profile and the HbA1c levels and a marked reduction in the number of hypoglycemic events.
Chandalia et al.56 also demonstrated that high-fibre diets contributed to better metabolic control in thirteen T2DM diabetic patients. In a cross-over study, patients were randomized to a diet containing a moderate amount of fibre (8 g of soluble fibre and 16 g insoluble fibre) or to a diet containing a high amount of fibre (25 g of soluble fibre and 25 g insoluble fibre). Plasma glucose concentrations were significantly lower for the high fibre diet than for the low-fibre diet56. In contrast, Jenkins et al.57 used a cross-over design to study the effects of a diet high in cereal fibre in T2DM patients and found no improvement in conventional markers of glycemic control after 3 months of intervention.
In clinical studies using fibre supplements, it appears that only the viscous variety of soluble fibre plays a significant role in reducing postprandial glycemia. This is in contrast to the findings from prospective studies where insoluble fibre, but not soluble fibre, from both of natural food source was inversely related to the risk of diabetes.45,46 However, a recent metaanalysis of prospective studies showed no major difference in the relative risk of diabetes for either soluble or insoluble fibre. This could be because the amount of soluble fibre consumed in an average diet is not sufficient to cause a significant effect.59
The most commonly studied fibre supplements in terms of their effect on the postprandial glucose and insulin response are Psyllium or Plantago ovata,60,61 glucomannan,62,63 guar gum64,65 and pectin.66,67 In almost all cases the intake of this type of fibre was associated with a better postprandial metabolic response, although this was not in case of Glore's study.64
Currently, the American Diabetes Association recommends that diabetic patients consume 14 g/1000 kcal/day of fibre because a high amount of fibre is necessary to improve glycemic control. This amount is between 2 and 3 times higher than that consumed by individuals in many developed countries.68
High fibre diets, in general, are well accepted and palatable for the majority of the population, as is observed in several prospective studies and clinical trials. However, long-term compliance with fibre supplemented diets is poor in adults. In addition, soluble fibre supplements are frequently associated with gastrointestinal complaints. If fibre is to be considered a long-term therapeutic option for diabetic patients in the future, an effective and well-tolerated source needs to be found.
In summary, the short term beneficial effects of fibre on the glycemic profile have been widely documented; however, there have not been enough trials to prove categorically that soluble fibre supplements would be an effective tool for ameliorating glycemic control in the long term. Although prospective studies have shown that fibre in the diet protects the individual from diabetes, clinical trials are necessary in the future to corroborate the beneficial effects of fibre in monitoring the incidence of diabetes.
Influence of fibre on the serum levels of cholesterol
Proposed mechanism of action
]]> Several mechanisms have been described in order to explain the effect of dietary fibre on blood lipid profile. In this sense, the hypocholesterolaemic action of fibre is partly mediated by a lower absorption of intestinal bile acid because the interruption of the enterohepatic bile acid circulation,69 thus increasing faecal bile acid loss, and its de novo synthesis in liver.70 Moreover, Fernández71 and Trautwein and co-workers72 suggested that the physicochemical properties of soluble fibre result in important modifications in volume, bulk and viscosity in the intestinal lumen, which will alter metabolic pathways of hepatic cholesterol and lipoprotein metabolism, also resulting in lowering of plasma LDLcholesterol. Other studies suggest that dietary fibre increases the enzymatic activity of cholesterol-7-α-hydroxylase, the major regulatory enzyme in the hepatic conversion of cholesterol to bile acids73 contributing to a higher depletion of hepatic cholesterol. Secondarily, this depletion leads to a stimulatory effect on the enzymatic activity of HMG-CoA reductase increasing the endogenous cholesterol synthesis. However, at the same time, there is an increase in the number of LDL-c receptors and in the recruitment of the esterified cholesterol from the circulating LDL-c particles. 74 Jenkins75 and Jones and coworkers76 described a reduction in the hepatic lipogenesis stimulated by insulin. It has also been suggested that the fermentation of dietary fibre by the intestinal microflora could modify the short chain fatty acids production thus reducing the acetate and increasing the propionate synthesis. This in turn reduces the endogenous synthesis of cholesterol, fatty acids and very low density lipoproteins.77,78Traditional dietary patterns, characterized by high fibre content, have been associated with lower rates of coronary disease. However, it should be taken into account that foods rich in fibre are also usually rich in a wide range of other bioactive substances which have a clear role in the prevention of cardiovascular disease.79-81 Likewise, the beneficial effect of diets enriched in fibre on the lipid profile could also be because these diets are traditional low in fat (especially saturated fat) or because they promote satiety and therefore help to protect against overweight and obesity.82
Observational and epidemiological studies
Cross-sectional studies have shown that a higher intake of dietary fibre is related to a best lipid profile (table V). Thus, for example, in an analysis of dietary factors and cardiovascular risk performed in a sample of 3,452 Swiss adults, it was observed that a healthy diet characterized by high consumption of dietary fibre was associated with lower rates of serum triglycerides and higher HDL-c.83 An improvement in lipid profiles associated to a high fibre consumption has also been observed in epidemiologic studies (see table V) carried out on adults in Germany,84 China,85 Denmark,86 France,87,88 Greece,89 Italy90 and Maryland.91 However, it is well known that can not be established any causal relationship through the results obtained in cross-sectional studies.
A ten year study of a cohort of 2,909 healthy adults aged between 18 and 30 showed a strong negative association between fibre intake and blood pressure and levels of triglyceride, high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, and fibrinogen even after adjusting for confounding factors. However these associations were substantially attenuated by adjustment for fasting insulin level suggesting that the effect of fibre on insulin metabolism could also explain the relationship between fibre dyslipidemia or cardiovascular disease.23 A similar study observed a decrease of 12.5 mg/dl in the serum total cholesterol levels (P < 0.05) for each increase of 10 g in the consumption of dietary fibre intake in a 7- year of follow-up in a cohort of 316 of Japanese-Brazilians subjects.92 Wu et al. 93 studied a cohort of 573 adults aged between 40 and 60 and found and inverse relationship between the ratio of TC/HDL-c and the total intake of dietary fibre (P = 0.01). This is important because the ratio of TC/HDL-c has been proposed as a good indicator of cardiovascular risk.94,95
Experimental and clinical studies
In relation to controlled and randomized clinical trials, since Keys and coworkers96 established for first time that some types of dietary fibre can decrease plasma total cholesterol in humans, several studies have shown that a high consumption of dietary fibre, particularly soluble fibre (pectin, guar gumm,b-glucans, glucomannan, psyllium), significantly decrease serum levels of TC and LDL-c.97,98 However, a meta-analysis carried out by Brown et al.99 indicates that the effects of different types of viscous fibres on TC concentrations are modest. These results were obtained from 67 experimental metabolic studies carried out on 2,990 subjects showing that for each gram of soluble fibre added to the diet, the TC and the LDL-c concentration decreased by 1.7 mg/dL and 2.2 mg/dL respectively.99
Epidemiological evidences showed a stronger association with cardiovascular protection of insoluble fibre than soluble fibre.7 In a recent parallel, doubleblind, placebo-controlled clinical trial, 200 overweight or obese patients were randomized to receive a mixed dose of soluble fibre (3 g Plantago ovata husk and 1 g glucomannan) or a placebo twice or three times daily in the context of an energy-restricted diet for a period of 16 weeks. Differences in plasma LDL-c changes between the groups were significant with greater reductions in the two fibre supplemented groups in comparison to the placebo. A similar pattern was observed for changes in TC: HDL-c and HDL-c: LDLc ratios.40 Others clinical trials support the hypocholesterolemic effects of soluble fibre derived both from supplements100-104 or fibre derived from foods105-110 (see table VI) on patients at high risk of cardiovascular disease. However, the efficacy of water-soluble fibre intake from oat bran in lowering serum lipid and glucose levels in a free-living population of healthy persons was not demonstrated.111 In a meta-analysis of 8 controlled trials, it was observed that the hypolipidemic effects of physillium in hypocholesterolemic individuals already consuming a low-fat diet beyond reductions achieved with diet only. Results confirm that psyllium significantly lowers an additional 4% of serum total and cholesterol and an additional 7% relative of LDL-c concentrations in comparisons to placebo group consuming a low fat diet.112 In relation to the effect of soluble fibre on HDL-c levels, there is some controversy in the literature. Thus while some studies shown a reduction of plasma HDL-c levels,113 and others report that it has little, no or an inconsistent effect on HDL-c.114
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Insoluble fibre such as that from wheat or cellulose has not been reported to have any significant effect on blood cholesterol,115,116 although as has been mentioned, various epidemiological studies show that the consumption of insoluble fibre is associated with a reduction in the risk of coronary diseases and T2DM, possibly because of the presence, along with dietary fibre, of several bioactive and antioxidant phytochemical substances in foodstuffs117 or because of the effect that fibre has on blood pressure, body weight and postprandial glycemia or insulin levels.93
In clinical practices, diets rich in fibre and dietary fibre supplements have been used to decrease plasma cholesterol and thus prevent cardiovascular diseases. The latest recommendations from the panel of American experts on cholesterol control (National Cholesterol Education Program-III, 2002) highlight the benefits of adding a variable quantity of soluble fibre (10-25 g/day) and phytosterols (2 g/day) to the diet as a primary or secondary prevention strategy to delay pharmacological treatment or to avoid unnecessary increases in the doses of hypolipidemic agents. The American Heart Association recommends a total dietary fibre intake of 25 g/day to 30 g/day from foods (not supplements) to ensure nutrient adequacy and maximize the cholesterol-lowering impact of a fatmodified diet.118 Finally, as has been mentioned, both the American Dietetic Association and the Institute of Medicine advise an intake of 14 g of dietary fibre per 1,000 kcal, or 25 g/day for adult women and 38 g/day for adult men, to protect against cardiovascular disease, and that this fibre should come from high-fibre foods.1,119
To conclude, the evidence available shows that the intake of foods that are high in fibre has clear benefits regarding the lipid profile and cardiovascular risk. Although some studies of fibre supplements have shown positive effects regarding the control of blood lipids, the number of adults who adhere to the use of fibre supplements tends to be low. Likewise, these effects are modest when compared with a whole foods approach that encourages the consumption of fibrerich foods.119-122 As was concluded at the last World Health Organization workshop on carbohydrates and human nutrition, the best sources of dietary fibre are intact fruits, vegetables, whole grains, nuts and pulses, all of which are rich in potentially cardioprotective components.82 Consequently, a Mediterranean-style diet rich in those foods should be recommended to improve the lipid profile and to reduce the risk of cardiovascular disease.123-124
Acknowledgments
The authors would like thank Carles Munné-Cuevas for the administrative and technical support provided.
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Correspondence:
Jordi Salas-Salvadó.
Human Nutrition Unit. ]]>
Department of Biochemistry and Biotechnology.
Faculty of Medicine and Health Sciences.
Rovira i Virgili University.
C/ Sant Llorenç, 21.
43201 Reus. Spain.
E-mail: jordi.salas@urv.cat
Recibido: 27-VII-2009.
Aceptado: 19-VIII-2009.