Role of Fiber in Cardiovascular Diseases: A Review

Authors

  • M. Viuda-Martos,

    1. Authors Viuda-Martos, López-Marcos, Fernández-López, Sendra, and Pérez-Álvarez are with IPOA Research Group (UMH-1 and REVIV-Generalitat Valenciana), AgroFood Technology Dept., Escuela Politécnica Superior de Orihuela, Univ. Miguel Hernández, Crta, Beniel km. 3,2, E-03312 Orihuela Alicante, Spain. Author López-Vargas is with Inst. de Ciencia y Tecnologia de Alimentos ICTA, Univ. Nacional de Colombia Sede Bogotá 3465000 ext. 19225, Bogota, Colombia. Direct inquiries to author Pérez-Alvarez (E-mail: ja.perez@umh.es).
    Search for more papers by this author
  • M.C. López-Marcos,

    1. Authors Viuda-Martos, López-Marcos, Fernández-López, Sendra, and Pérez-Álvarez are with IPOA Research Group (UMH-1 and REVIV-Generalitat Valenciana), AgroFood Technology Dept., Escuela Politécnica Superior de Orihuela, Univ. Miguel Hernández, Crta, Beniel km. 3,2, E-03312 Orihuela Alicante, Spain. Author López-Vargas is with Inst. de Ciencia y Tecnologia de Alimentos ICTA, Univ. Nacional de Colombia Sede Bogotá 3465000 ext. 19225, Bogota, Colombia. Direct inquiries to author Pérez-Alvarez (E-mail: ja.perez@umh.es).
    Search for more papers by this author
  • J. Fernández-López,

    1. Authors Viuda-Martos, López-Marcos, Fernández-López, Sendra, and Pérez-Álvarez are with IPOA Research Group (UMH-1 and REVIV-Generalitat Valenciana), AgroFood Technology Dept., Escuela Politécnica Superior de Orihuela, Univ. Miguel Hernández, Crta, Beniel km. 3,2, E-03312 Orihuela Alicante, Spain. Author López-Vargas is with Inst. de Ciencia y Tecnologia de Alimentos ICTA, Univ. Nacional de Colombia Sede Bogotá 3465000 ext. 19225, Bogota, Colombia. Direct inquiries to author Pérez-Alvarez (E-mail: ja.perez@umh.es).
    Search for more papers by this author
  • E. Sendra,

    1. Authors Viuda-Martos, López-Marcos, Fernández-López, Sendra, and Pérez-Álvarez are with IPOA Research Group (UMH-1 and REVIV-Generalitat Valenciana), AgroFood Technology Dept., Escuela Politécnica Superior de Orihuela, Univ. Miguel Hernández, Crta, Beniel km. 3,2, E-03312 Orihuela Alicante, Spain. Author López-Vargas is with Inst. de Ciencia y Tecnologia de Alimentos ICTA, Univ. Nacional de Colombia Sede Bogotá 3465000 ext. 19225, Bogota, Colombia. Direct inquiries to author Pérez-Alvarez (E-mail: ja.perez@umh.es).
    Search for more papers by this author
  • J.H. López-Vargas,

    1. Authors Viuda-Martos, López-Marcos, Fernández-López, Sendra, and Pérez-Álvarez are with IPOA Research Group (UMH-1 and REVIV-Generalitat Valenciana), AgroFood Technology Dept., Escuela Politécnica Superior de Orihuela, Univ. Miguel Hernández, Crta, Beniel km. 3,2, E-03312 Orihuela Alicante, Spain. Author López-Vargas is with Inst. de Ciencia y Tecnologia de Alimentos ICTA, Univ. Nacional de Colombia Sede Bogotá 3465000 ext. 19225, Bogota, Colombia. Direct inquiries to author Pérez-Alvarez (E-mail: ja.perez@umh.es).
    Search for more papers by this author
  • J.A. Pérez-Álvarez

    1. Authors Viuda-Martos, López-Marcos, Fernández-López, Sendra, and Pérez-Álvarez are with IPOA Research Group (UMH-1 and REVIV-Generalitat Valenciana), AgroFood Technology Dept., Escuela Politécnica Superior de Orihuela, Univ. Miguel Hernández, Crta, Beniel km. 3,2, E-03312 Orihuela Alicante, Spain. Author López-Vargas is with Inst. de Ciencia y Tecnologia de Alimentos ICTA, Univ. Nacional de Colombia Sede Bogotá 3465000 ext. 19225, Bogota, Colombia. Direct inquiries to author Pérez-Alvarez (E-mail: ja.perez@umh.es).
    Search for more papers by this author

Abstract

ABSTRACT:  Worldwide, cardiovascular disease is estimated to be the leading cause of death and loss of disability-adjusted life-years. Effective prevention needs a global strategy based on knowledge of the importance of risk factors, including diet. Recent years have seen increased interest on the part of consumers, researchers, and the food industry into how food products can help maintain the health of an individual. Extracts rich in dietary fiber obtained from plants could be used as functional ingredients because they provide numerous health benefits that go far beyond supporting bowel regularity. These benefits may include not only digestive health, but weight management, cardiovascular health, and general wellness. The objective of this review is to present an overview of the potential of different types of fiber as a technological tool for its application to functional foods to reduce the incidence of cardiovascular disease through diet.

Introduction

Recent knowledge supports the hypotheses that, besides fulfilling nutrition needs, diet modulates various functions in the body and may exhibit detrimental or beneficial roles in some diseases (Sarkar 2007). The increase in consumer demand for high-quality food products has led to growth in the use of new technologies and ingredients. Several factors that influence changes in consumer demand, including: health concerns such as cholesterol, cancer, obesity; changes in demographic characteristics such as ethnicity, population aging; changes in distribution systems and price; and the need for convenience (Pérez-Alvarez 2008a). In recent years, a considerable growing interest towards natural and wholesome foods has been developed among consumers throughout the world, leading to nutrition science research relating to the association between diet and dietary constituents and health benefits, favorable regulatory environment, consumer self-care phenomena, and rapid growth in the market for health and wellness products (Hasler 2002). Actually, considerable importance is given to functional foods, which, in principle, apart from their basic nutritional functions, provide physiological benefits, play an important role in disease prevention, or slow the progress of chronic diseases. Functional foods either contain (or add) a component with a positive health effect or eliminate a component with a negative one. The relationship between diet and health has focused on the role of food choices and diseases like cancer, cardiovascular disease, and allergies (Lambert 2001). The market for functional foods is increasing at an annual rate of 15% to 20% (Hilliam 2000). To develop these types of products, one must evaluate consumer perceptions, the most important quality aspects being that they taste good, appear wholesome, and have nutritional value (García-Segovia and others 2007). Also, Pérez-Alvarez (2008a) describes that any functional food must be safe, healthy, and tasty. Many components may be added to foods to make them “functional” including ω-3 fatty acids (Hjaltason and Haraldsson 2006), vitamins (Baro and others 2003), probiotics (Salem and others 2006), prebiotics (Brink and others 2005), symbiotics (D’Antoni and others 2004), phytochemicals (Wolfs and others 2006), bioactive peptides (Thoma-Worringer and others 2006), fiber (Fernández-Ginés and others 2004; Fernández-López and others 2007, 2008, 2009), and so on.

Dietary fiber intake in Western countries is currently estimated to be 25 g per person per day. However, nutritionists recommend an intake of 35 g per person per day (Lairon 1990). The development of fiber-enriched foods would help consumers to meet such recommendations. Since the roles of dietary fibers in preventing and treating some diseases have been well documented, the addition of purified dietary fibers to foods has become popular. Different types of dietary fibers, such as pea, apple, sugar beet, soy, and citrus fibers, as well as inulin and gums, are now incorporated into foods for their nutritional properties or for their functional and technological properties (Thebaudin and others 1997). From a functionality point of view, fiber can play a number of roles: (i) it may be used as a tool for improving texture, (ii) as a bulking agent in reduced-sugar applications, (iii) to manage moisture in the replacement of fat, (iv) to add color, and (v) as natural antioxidant.

Although fiber itself may be invisible in food products, it is fast becoming one of the most appreciated ingredients in today's marketplace. In 2007, consumers ranked fiber number 5 among the top 10 functional food concepts (Sloan 2008).

The objective of this review is to present an overview of the potential of different types of fiber as a technological tool to use in functional foods to reduce the incidence of cardiovascular disease through diet.

Incidence of Cardiovascular Diseases in Western Countries

Cardiovascular diseases (CVDs) are among the most common causes of death and disability worldwide (Goyal and Yusuf 2006). CVDs include coronary heart disease (heart attacks), cerebrovascular disease (strokes), high blood pressure (hypertension), peripheral artery disease, heart rhythm problems (arrhythmias), rheumatic heart disease, congenital heart disease, and heart failure (WHO 2009a). According to the World Health Org., the standardized CVD mortality rates vary considerably from country to country in the developed world, with Mediterranean countries and Japan having the lowest rates (WHO 1990). Globally, cardiovascular diseases are the number one cause of death and are projected to remain so. An estimated 17.5 million people died from cardiovascular diseases in 2005, representing 30% of all global deaths. Of these deaths, 7.6 million were due to heart attacks and 5.7 million to stroke. About 80% of these deaths occurred in low- and middle-income countries. If current trends are allowed to continue, by 2015 an estimated 20 million people will die annually from cardiovascular disease (mainly from heart attacks and strokes) (WHO 2009b). In the beginning of the 20th century, results of observational studies suggested that cardiovascular disease was originally more common in the upper socio-economic stratum (Bucher and Ragland 1995). However, after the middle of the 20th century this gradually changed, especially in westernized countries, so that, currently, CVD is more common in the lower socio- economic status groups (Manios and others 2005). Groups with lower socio-economic status tend to adopt unhealthier behavior, such as smoking and careless dietary habits, and seem to have a worsened psychological profile and an increased prevalence of the common CVD risk factors (Panagiotakos and others 2008).

Risk Factors

Risk assessment for the primary prevention of CVD and stroke should include regularly updated family history, smoking status, food intake and nutrition patterns, alcohol intake, physical activity, blood pressure, body mass index (BMI), waist circumference, pulse rate, fasting serum lipoprotein profile (or total and HDL cholesterol if fasting is unavailable), and fasting blood glucose level (Pearson and others 2002).

Studies that have considered multiple risk factors include the Framingham study, where the risk for cardiovascular diseases was summarized into a single measure that integrated smoking and a set of clinical measures (Kannel and Gordon 1974). More recently, the Chronic Disease Risk Index (CDRI), a semiquantitative composite measure, combined rankings for smoking, alcohol use, body mass index, fat intake, and fruit and vegetable consumption (Meng and others 1994). There are numerous risk factors in CVDs such as age, body weight, physical inactivity, blood pressure, cigarette smoking, alcohol intake, and dyslipidemia (Do and others 2000).

Obesity

Obesity is an independent risk factor for CVD. According to the World Health Org., there are currently more than 1 billion overweight adults, 300 million of whom are obese (Mackay and Mensah 2004). The INTERHEART study, which enrolled almost 30000 men and women in 52 countries, reported that a waist-to-hip ratio greater than the cut-off of 0.83 for women and 0.9 for men resulted in a 3-fold increase in population attributable risk for myocardial infarction (Yusuf and others 2004).

Physical inactivity

The literature consistently indicates that a sedentary lifestyle increases the risk of developing several chronic diseases and conditions, while regular physical activity enhances overall health (Belahsen and Rguibi 2006). Physical activity includes any bodily movements produced by skeletal muscles that result in energy expenditure, covering daily walking activities at work and structured exercise training (Pettman and others 2008). To reduce the risk of CVD, people need at least 150 min of moderate-intensity aerobic physical activity per week or at least 90 min of vigorous aerobic exercise per week (Franzini-Pereira and Franz 2008).

Blood pressure

High blood pressure (BP) is one of the most prevalent cardiovascular risk factors and the single greatest contributor to cardiovascular disease worldwide (López and others 2006). High BP commonly clusters with other cardiovascular risk factors, such as metabolic syndrome (Malik and others 2004). Lifestyle factors that may lower blood pressure are sodium restriction, weight reduction or physical activity programs, and a reduction of excessive alcohol intake (Watkins 2003).

Smoking

Cigarette smoking is an avoidable risk factor for CVD. An estimated 34.7% of all deaths resulting from cigarette smoking are related to CVD. Strong evidence links consumption of tobacco with increases in low-density lipoprotein cholesterol (LDL-C) oxidation, platelet aggregation, and endothelial impairment (Bloomer 2007). Smoking increases the risk for developing atherosclerosis, hypertension, and stroke, and it is the most important preventable cause of premature death (AHA 2008).

Alcohol intake

Moderate alcohol consumption, typically defined as up to 2 drinks per day for men and 1 drink per day for women, has been consistently associated with lower risk of coronary heart disease in observational studies. At least 2 meta-analyses have come to consistent conclusions about the magnitude of this association (Corrao and others 2000) and it is further supported by the established beneficial effects of moderate drinking on high-density lipoprotein cholesterol and other cardiovascular risk factors (Watzl and others 2002). However, excess in alcohol consumption has detrimental health effects on blood pressure and triglyceride levels (Wakabayashi 2009).

Dyslipidemia

One of the major risk factors for the development of coronary heart disease is dyslipidemia, mainly characterized by elevated levels of low-density lipoprotein cholesterol (LDL-C) and/or reduced high-density lipoprotein cholesterol (HDL-C) (Esmaillzadeh and Azadbakht 2008). Epidemiological studies have shown that high concentrations of serum total cholesterol and low-density lipoprotein cholesterol (LDL-C) are independent risk factors for CVD (Russo and others 2008). Plasma concentrations of LDL and cholesterol are influenced by both genetic and environmental factors (Mirmiran and others 2009).

Diet and Cardiovascular Diseases

It is well established that nutrition can have a direct impact on normal physiological functioning, as well as on pathological conditions such as obesity, hypertension, diabetes, and cardiovascular disease (Maurer and others 2009). The prevalence of CVD ranges between 2% and 10% in southern European countries, in contrast to the 10% to 18% in Northern European countries (Keys and others 1986). Several scientists during recent years have attributed, at least in part, the differences in mortality rates between various countries of the world to the quite different nutritional habits of populations (WHO 1990). The intake of energy and nutrients in Southern European countries is similar to that in diets of North European countries and an excess of total energy provided to a large extent by fat and protein at the expense of carbohydrates (Saura-Calixto and Goñi 2009). However, there are differences between Southern and Northern European countries in relation to fat consumption. Southern European countries consume much more olive oil and unprocessed red meats, while Central and Northern Europeans preferably consume processed meat products (Naska and others 2006). The overconsumption of a maladaptive, westernized diet consisting of foods that are calorie-dense, nutritionally-poor, phytochemical-depleted, highly processed, and rapidly absorbable has been shown to increase systemic inflammation and reduce insulin sensitivity (Fito and others 2007).

With chronic ingestion, this dietary pattern often results in metabolic syndrome (MetS), a physiological state encompassing a cluster of metabolic abnormalities, including dyslipidemia, central obesity, hypertension, and glucose intolerance. These are all independent risk factors for the development of type 2 diabetes and/or cardiovascular disease (Moller and Kaufman 2005).

Conversely, the various lifestyle and dietary interventions that affect plasma cholesterol and triglyceride levels are usually considered effective in cardiovascular risk reduction such as (Poli and others 2008):

  • (i) Modify the pattern of consumption of dietary fatty acids;
  • (ii) Reduce the dietary intake of cholesterol;
  • (iii) Modify the pattern of consumption of carbohydrates and fiber;
  • (iv) Change the proportional intake of other micronutrients and macronutrients;
  • (v) Manage weight;
  • (vi) Supplement the diet with phytosterol-enriched foods or soy protein;
  • (vii) Take regular exercise.

Adherence to the traditional Mediterranean diet, characteristically rich in fruits, vegetables, bread, cereals, potatoes, beans, nuts, seeds, olive oil (as an important fat source), dairy products, and fish, along with low to moderate amounts of poultry, little red meat, and modest consumption of red wine with meals (Kris-Etherton and others 2002; Perez-Alvarez and Aleson-Carbonell 2003), has been associated with a reduction in CVD (Trichopoulou and others 2003). This protective effect has been attributed, at least in part, to the Mediterranean-style diet, low in processed foods and refined carbohydrates and high in monounsaturated fatty acids and plant foods that provide a large amount of natural antioxidants (Trichopoulou and others 2003; Ebbeling and others 2005). Brighenti and others (2005) reported that total antioxidant capacity is inversely and independently correlated with plasma concentrations of highly sensitive C-reactive protein, and this could be one of the mechanisms whereby antioxidant-rich foods, present in the Mediterranean diet pattern, protect against cardiovascular disease. Fito and others (2007) reported that the Mediterranean diet pattern promoted benefits in classic and novel risk factors for CVD because a decrease in the oxidative damage to LDL to be one of the protective mechanisms by which the Mediterranean diet could exert protective effects on CVD development. Robust clinical evidence exists indicating that the Mediterranean diet may be cardioprotective, positively impacting the clinical progression of CVD, reducing the risk of CVD (by 8% to 45%), and attenuating the cardiovascular complications after a myocardial infarction (De Lorgeril and Salen 2006). The Mediterranean diet need to be better defined if guidelines, useful to modern societies, are to be formulated. Researchers and policy makers should decide whether the Mediterranean diet should be promoted as a “nutrient profile” or as a “food selection pattern” (Anonymous 2009).

Functional Food in Cardiovascular Diseases

Recent years have seen increased interest on the part of consumers, researchers, and the food industry into how food products can help maintain the health of the organism, while the role that diet plays in the prevention and treatment of many illnesses has become widely accepted (Viuda-Martos and others 2009). The classical concept of “adequate nutrition,” that is, the provision of nutrients (carbohydrates, proteins, fats, vitamins, and minerals) is slowly being replaced by the concept of “optimal nutrition,” which, besides the components mentioned previously, includes the potentiality of foods to promote health, improve well-being, and reduce the risk of developing disease (Pérez-Alvarez 2008a); hence, the appearance of terms likes functional foods, designed or therapeutic foods, superfoods, pharmafoods, or medicinal foods (Nagai and Inoue 2004). There is no one definition for the term functional food. Indeed, the concept of functional food is complex and may refer to many possible aspects, including food obtained by any process, whose particular characteristic is that one or more of its components, whether or not that component is itself a nutrient, affects the target function of the organism in a specific and positive way, or promotes a physiological or psychological effect beyond the merely nutritional (Viuda-Martos and others 2009). The food industry and scientific community use the term functional foods to refer to products with health benefit claims beyond their inherent nutritional value (Nestle 2002). In general, 2 types of health claims can be distinguished; first, claims referring to enhance body function, and second, those that refer to a reduced risk of disease measured by an intermediate biomarker such as cholesterol level, blood pressure, or satiety (Wieringa and others 2008).

The ILSI Europe (1999) has established that “a food product can be considered as functional if it has satisfactorily been proved that it produces a beneficial effect on one or more physiological functions, besides its conventional nutritional effects, this being relevant for improving human health and/or reducing the risk of suffering certain diseases.”Doyon and Labrecque (2008), together with a group of experts from North America and Europe, redefined the definition of functional foods using the Delphi technique. Functional food is now defined as food that is or appears similar to a conventional food. It must be a part of the standard diet, which is consumed on a regular basis and in normal quantities. Other than that, it should also have been proven to reduce the risk of specific chronic diseases or beneficially affect target functions beyond basic nutritional functions.

There are a large number of foods that can be considered functional foods, such as fruits and vegetables, olive oil, cereals, red wine, fish, and so on, since among their components there are many that can prevent or delay several diseases including CVD.

Fruits and vegetables

Fruits and vegetables contain constituents, notably vitamins, minerals, and dietary fiber, which are essential to a healthy, well-balanced diet. Furthermore, it has been shown that some of the secondary metabolites of fruits and vegetables, such as flavonoids and carotenoids, have a beneficial effect on health by directly combating the onset of cancer and CVD (Fernández-Ginés 2003). Indeed, Mirmiran and others (2009) reported that the consumption of fruits and vegetables is associated with lower concentrations of LDL and the risk of CVD in a dose-response manner, while Suido and others (2002) indicated that fruit and vegetable consumption decreased LDL concentrations in hypercholesterolemic subjects.

Olive oil

Olive oil may produce its dietary health benefits by lowering blood pressure (Psaltopoulou and others 2004) and by contributing to a proper lipid intake in 2 ways: directly by increasing monounsaturated lipids, and indirectly by decreasing saturated lipid intake. It has also been widely suggested that the beneficial effects of olive oil derive not only from its high oleic content but also from the presence of polyphenolic antioxidants (Sánchez-Zapata and Pérez-Alvarez 2008); however, other resaerchers consider that intake of olive oil phenols is probably too low to produce a measurable effect on oxidation markers in humans (Vissers and others 2004).

Cereals

There is convincing evidence that the consumption of whole grain foods is associated with reduced incidences of chronic diseases, including diabetes, cardiovascular disease, and certain cancers (Katcher and others 2008). In addition to dietary fiber, various phytochemicals, vitamins, and minerals have been suggested to contribute to the health effects of whole grain foods (Slavin 2003).

Red wine

Resveratrol, a polyphenolic constituent of grapes and red wine, has been reported to have atheroprotective and hypolipidemic properties (Norata and others 2007). It has been suggested that the antioxidant properties of resveratrol protect against lipoprotein oxidation and foam cell formation while promoting cholesterol efflux from macrophages, are responsible for the protective effect against CVD of consuming moderate amounts of red wine (Berrougui and others 2009).

Fish

There is evidence that the consumption of approximately 2 servings of fish per week (approximately 224 g total) reduces the risk of mortality from coronary heart disease and that consuming eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) may reduce the risk of mortality from cardiovascular disease in people who have already experienced a cardiac event (Inst. of Medicine 2005).

Functional Ingredients in Cardiovascular Diseases

Omega-3 Fatty Acids

Omega-3 fatty acids are polyunsaturated fatty acids of which 3 main types are found in the human diet: alpha-linolenic acid (ALA), docosahexaenoic acid (DHA), and eicosapentaenoic acid (EPA) (Bent and others 2009). DHA and EPA are found in seafood, while ALA is found in nut and plant oils. Interestingly, fish do not produce EPA and DHA, but the oils are synthesized by single-cell marine organisms that are eaten by fish (Harris 2004). These 3 substances, DHA, EPA, and ALA, are typically considered essential human nutrients and are often called ‘‘essential fatty acids’’ (Freeman and others 2006). Omega-3 fatty acids are suggested to exert various beneficial effects including antiinflammatory properties and reduction in blood triacylglycerol levels, prevention of cardiac arrhythmias, stabilization of atherosclerotic plaques, reduction in platelet aggregation, reduction in blood pressure, and improved arterial compliance (Holub 2002; Kris-Etherton and others 2002). To produce these beneficial effects the blood must have a high omega-3 index. The omega-3 index is a relatively new concept, defined as the sum of EPA and DHA expressed as a percentage of the total fatty acid content of red blood cell membranes (Harris and Von 2004).

Omega-3 fatty acids, either as a supplement or when consumed as oily fish, have many beneficial effects (McCombie and others 2009). A great variety of foods including chicken meat (López-Ferrer and others 2001), pork (Howe and others 2002), eggs (Lewis and others 2000), bread (Yep and others 2002), spreads (Kolanowski and others 2001), and other processed products (Metcalf and others 2003) have been enriched with omega-3 fatty acids.

Bioactive Compounds

Nowadays, it is widely accepted that the beneficial health effects of fruits and vegetables in the prevention of heart disease and certain types of cancer are due to their bioactive components (Galaverna and others 2008). The presence of significant amounts of bioactive compounds, such as phenolic acids, flavonoids, and carotenoids, in DF from fruits assures them considerable nutritional value (Saura-Calixto and Goñi 2005). The antioxidant properties of flavonoids and carotenoids come from their ability to link free radicals that easily attack saturated fatty acids present in cell membranes, causing peroxidation, decreased permeation, and damage of membrane proteins, leading to cellular inactivation. DNA is also subject to free radical-effects producing mutations which may lead to cancer (Ubando and others 2005).

Phenolic acids and flavonoids

One of the main compounds responsible for most of the functional properties of many foods, among them fruits and vegetables, are phenolic compounds in any of their forms, whether simple phenols, flavones, flavanones, flavanols, flavonols, anthocyanins, and so on (Viuda-Martos and others 2009). Phenolic compounds are found in most plants and in many cases they contribute to their color and taste (Belitz and Grosch 1997). Chemically, phenolic acids can be defined as substances that possess an aromatic ring bound to one or more hydrogenated substituents, including their functional derivates (Marín and others 2001).

Flavonoids are low-molecular-weight compounds consisting of 15 carbon atoms, arranged in a C6-C3-C6 configuration. Essentially, the structure consists of 2 aromatic rings joined by a 3-carbon bridge, usually in the form of a heterocyclic ring (Balasundram and others 2006).

Phenolic acids and flavonoids have been associated with the health benefits derived from consuming high levels of fruits and vegetables (Parr and Bolwell 2000). The beneficial effects derived from phenolic acid and flavonoids, with respect to CVD prevention have been attributed to (i) their antioxidant activity (Heim and others 2002), (ii) the prevention of atherosclerosis (Tripoli and others 2007), and (iii) the effect on platelet aggregation (Lamuela-Raventos and others 2005).

The antioxidant activity of phenolic acids and flavonoids arises from the scavenging of free radicals, hydrogen donation, metallic ion chelation, or even acting as substrate for radicals like superoxide or hydroxyl (Al-Mamary and others 2002; Amarowicz and others 2004). These bioactive compounds with antioxidant properties also interfere with propagation reactions (Russo and others 2000) and inhibit the enzymatic systems involved in initiation reactions (You and others 1999).

In vitro, flavonoids inhibit the oxidation of low-density lipoprotein (LDL) and reduce thrombotic tendencies (Benavente-García and others 1997). Using animal models of atherosclerosis Grassi and others (2008) has indicated that dietary flavonoid consumption delays atherosclerotic plaque development and may reduce endothelial dysfunction, which is the key step in the development of atherosclerosis. Hodgson (2008) reported that flavonoids inhibit the development of atherosclerosis in animal models. Choi and others (2008) suggested that (-)epigallocatechin gallate and hesperetin, both flavonoids, may act as antiatherogenic agents by blocking oxidized LDL-induced endothelial apoptosis via differential cellular apoptotic mechanisms.

The 3rd way which helps prevent CVD is through the effect of phenolic acids and flavonoids on platelet aggregation. Furusawa and others (2003) reported that the interaction of flavonoids with membrane lipids, thus modifying membrane fluidity, appeared to be partly responsible for the antiaggregatory and disaggregatory effects on human platelets. Navarro-Núñez and others (2009) showed that flavonoids inhibit platelet function through several mechanisms, including the antagonism of specific membrane receptors in these cells.

Carotenoids

Carotenoids are a class of natural pigments, well know for the orange-red to yellow colors they impart to many fruits, vegetables, and flowers as well as for their provitamin A activity that some of them possess (Ribayamercado and others 2000). These compounds are polyenoic terpenoids having conjugated trans double bonds. They include carotenes (β-carotene and lycopene), which are polyene hydrocarbons, and xanthophylls (lutein, zeaxanthin, capsanthin, canthaxanthin, astaxanthin, and violaxanthin) that have oxygen in the form of hydroxy, oxo, or epoxy groups (Choe and Min 2009).

The majority of the 600 carotenoids found in nature are 40 carbons in length and may be pure hydrocarbons, called carotenes, or possess oxygenated functional groups, in which case they are called xanthophylls (Krinsky 1998).

The long-chain conjugated polyene structure accounts for the ability of these compounds to absorb visible light, but that also makes them quite susceptible to oxidation. This latter property is closely related to their ability to act as antioxidants (Reboul and others 2007). The properties, and therefore functions, of a carotenoid molecule are primarily dependent upon its structure and hence its chemistry (Young and Lowe 2001). In particular, the conjugated C = C double bond system is considered to be the single most important factor in energy transfer reactions, such as those found in photosynthesis (Christensen 1999). In human plasma and tissues, a wide range of carotenoids have been identified including cyclic (such as beta-carotene and alpha-carotene) and acyclic carotenes (such as lycopene and phytoene), together with a number of xanthophylls (such as zeaxanthin, lutein, and beta-cryptoxanthin), all of which can be directly derived from dietary sources (Khachik and others 1997).

Smoking and obesity, both established CVD risk factors, are associated with lower serum carotenoid concentrations, (Kritchevsky 1999). High plasma or adipose carotenoid concentrations have been potentially associated with a reduced risk of CVD (Street and others 1994) since the carotenoids, as potent antioxidants, retard the proliferation of free radicals and protect against free radical-mediated tissue damage (Svilaas and others 2004).

Dietary Fiber

Definition

At present, many aspects of properties and functions of dietary fiber (DF) remain unclear. Botanists define fiber as a part of plant organs, chemical analysts as a group of chemical compounds, and consumers as a substance with beneficial effects on human health, while for the dietetic and chemical industries DF is a subject of marketing (Rodríguez and others 2006). The concept of dietary fiber may have several definitions, depending on the specific study, but most researchers define it in terms of its effects on the human gastrointestinal tract and not something purely chemical or physical, or based on analytical methodologies for its determination (García-Ochoa and others 2008).

Traditionally, DF was defined as plant polysaccharides and lignin which are resistant to hydrolysis by the human digestive enzymes (Trowell and others 1976). However, this definition has changed with time. Thus, Stear (1990) defines dietary fiber as the food fraction that is not enzymatically degraded within the human gastro-alimentary tract and it is composed mainly of cellulose and lignin, but also of hemicelluloses, pectins, gums, and other carbohydrates. For Selvendran and Robertson (1994) fiber is “the group of nonstarch polysaccharides and lignin, which includes several indigestible polysaccharides in addition to the main components of the cell wall.”Prosky (2001) defines fiber as “that fraction of the edible part of plants or their extracts, or synthetic analogs that are resistant to digestion and absorption in the small intestine, usually with complete or partial fermentation in the large intestine.” The AACC (2001) defined DF as “the edible part of plants or analogous carbohydrates that are resistant to digestion and absorption in the human small intestine with complete or partial fermentation in the large intestine. That includes polysaccharides, oligosaccharides, lignin, and associated plant substances.”

The Inst. of Medicine (2002) has defined dietary fiber as “nondigestible carbohydrates and lignin that are intrinsic and intact in plants.” Added fiber consists of isolated, nondigestible carbohydrates that have beneficial physiological effects in humans. Total fiber is the sum of dietary fiber and added fiber. The United Kingdom IFST (2007) defines fiber as “food material, particularly plant material, that is not hydrolyzed by enzymes secreted by the human digestive tract but that may be digested by microflora in the gut. Plant components that fall within this definition include nonstarch polysaccharides (NSP) such as celluloses, some hemicelluloses, gums, and pectins, as well as lignin, resistant dextrins, and resistant starches.” For the European Commission (2008)“fiber” means carbohydrate polymers with 3 or more monomeric units, which are neither digested nor absorbed in the human small intestine and belong to the following categories:

  • (i) Edible carbohydrate polymers naturally occurring in the food consumed;
  • (ii) Edible carbohydrate polymers that have been obtained from food raw materials by physical, enzymatic, or chemical means and that have a beneficial physiological effect as demonstrated by generally accepted scientific evidence;
  • (iii) Edible synthetic carbohydrate polymers which have a beneficial physiological effect as demonstrated by generally accepted scientific evidence.

Given the confusion which is generated by conflicting definitions, and the potentially important role of fiber in protecting against and managing a wide range of diseases, an important consensus was reached at a meeting in South Africa of the Codex Alimentarius Committee on Nutrition and Foods for Special Dietary Uses (CCNFSDU) in November 2008. In this meeting, the World Health Org. and Food and Agriculture Org. defined fiber as carbohydrate polymers with 10 or more monomeric units, which are not hydrolyzed by the endogenous enzymes in the small intestine of humans and belong to the following categories:

  • (i) Edible carbohydrate polymers naturally occurring in the food as consumed;
  • (ii) Carbohydrate polymers, which have been obtained from food raw materials by physical, enzymatic, or chemical means and which have been shown to have a physiological effect of benefit to health as demonstrated by generally accepted scientific evidence to competent authorities;
  • (iii) Synthetic carbohydrate polymers which have been shown to have a physiological effect of benefit to health as demonstrated by generally accepted scientific evidence to competent authorities.

Classification

Dietary fiber is composed of total dietary fiber (TDF), which includes both soluble (SDF) and insoluble dietary fiber (IDF) (Wang and others 2002). Because solubility refers simply to fibers that are dispersible in water, the term is somewhat inaccurate (Figuerola and others 2005). Originally it was thought that this categorization might provide a simple way to predict physiological function, but this has not always been the case (Gallaher and Schneeman 2001). Figure 1 shows a classification of DF.

Figure 1—.

Classification of dietary fiber.

The structural or nonviscous fibers (lignin, cellulose, and some hemicelluloses) are water-insoluble. Vegetables and cereal grains are especially rich in water-insoluble fiber, with the highest amounts in wheat and corn. Water-insoluble fiber is responsible for increased stool bulk and helps to regulate bowel movements. The natural gel-forming or viscous fibers (pectins, gums, mucilages, algal polysaccharides, some storage polysaccharides, and some hemicelluloses) are water-soluble. Foods rich in water-soluble fiber are dried beans, oats, barley, and some fruits and vegetables (Grigelmo-Miguel and others 1999). Table 1 shows the origin, chemical component, description, and principal types of fiber.

Table 1—.  Types of dietary fiber, its description, and principal sources.
OriginChemical componentDescriptionSources
  1. Sources: Dutta and others (2009); Mermelstein (2009); Sharma and others (2008); Lunn and Buttriss (2007); Charalampopoulos and others (2002); Tharanathan (2002); Willför and others (2009); Trinidad and others (2006).

PlantCellulosePolysaccharides comprising up to 10000 closely packed glucose units, arranged linearly, making cellulose very insoluble and resistant to digestion by human enzymes.Principal component of the cell walls of most plants. Forms about 25% of the fiber in grains and fruit and about a third in vegetables and nuts. Much of the fiber in cereal bran is cellulose.
HemicellulosePolysaccharides containing sugars other than glucose. Associated with cellulose in cell walls and present in both soluble and insoluble forms.Forms about a third of the fiber in vegetables, fruits, legumes, and nuts. The main dietary sources are cereal grains.
LigninThree-dimensional network of coupled monomers of a varied 4-hydroxyphenylpropanoid type.Foods with a woody component; for example, celery, and the outer layers of cereal grains.
Resistant starchPolysaccharides composed of linear α-1,4-D-glucan, essentially derived from retrograded amylase fraction.Whole grains, legumes, cooked and chilled pasta, potatoes, rice, and unripe bananas.
GlucomannanA highly branched polysaccharide, soluble, fermentable, and viscous dietary fiber.Derived from the root of the elephant yam or konjac plant.
β-GlucansUnbranched polysaccharides composed of (1-4) and (1-3) linked β-D-glucopyranosyl units in varying proportions.Major component of cell wall material in oats and barley, only present in small amounts in wheat.
PectinPolysaccharides comprising galacturonic acid and a variety of sugars; soluble in hot water and forms gels on cooling.Found in cell walls and intracellular tissue of fruits and vegetables. Fruits contain the most, but pectins also represent 15% to 20% of the fiber in vegetables, legumes, and nuts.
GumsHydrocolloids derived from plant exudates.Plant exudates (gum arabic and tragacanth), seeds (guar and locust beans), and seaweed extracts (agar, carrageenans, alginates).
Uronic acidPolysaccharides comprising β-D-glucuronic acid, β-D-galacturonic acid, β-D-4-O-methylglucuronic acid.Found in cell wall of higher plants.
MucilagesPresent in the cells of the outer layers of seeds of the plantain family.Psyllium (Plantago ovata)
OligosaccharidesPolysaccharides consisting of 3 to 15 monosaccharide units.Pulses, onions, Jerusalem artichokes, garlic, and more.
AnimalChitosanLinear polysaccharide consisting of (1,4)-linked 2-amino-deoxy-b-D-glucan, deacetylated derivative of chitin.Mainly obtained from crustacean shells, also certain fungi, is the 2nd-most abundant natural polymer in nature after cellulose.
SyntheticResistant maltodextrinsTypically produced by purposeful rearrangement of starch or hydrolyzed starch to convert a portion of the normal alpha-1,4-glucose linkages to random 1,2-, 1,3-, and 1,4-alpha or beta linkages. 

Pectins are amorphous polysaccharides formed by the joining of galacturonic acid with different monosaccharides, mainly rhamnose, furans, xylose, and galactose. They have a great power to transform a hydrophilic viscous gel capable of forming gels in the presence of sugar, heat, and weak acid. These substances are present in the soft tissues of fruits (García and others 1995).

Guar gum is a galactomannan storage polysaccharide made up of polymers comprised of about 10000 molecules. The fiber consists of a (1→4)-linked-β-D-mannopyranose backbone with (1→6)-linked-α-D-galactose side chains. The overall ratio of mannose to galactose is around 2:1. Guar gum is an economical thickener and stabilizer. It hydrates easily in cold water giving a highly viscous solution (Theuwissen and Mensink 2008).

Cellulose is the main structural component that provides strength and stability to plant cell walls and fiber (Paster and others 2003). The amount of cellulose in a fiber influences the properties, economics of fiber production, and the utility of the fiber for various applications.

Hemicellulose in plants is slightly cross-linked and is composed of multiple polysaccharide polymers with a degree of polymerization and orientation less than that of cellulose (Rowell and others 1997). Hemicellulose usually acts as a filler between cellulose and lignin and consists of sugars including glucose, xylose, galactose, arabinose, and mannose (Reddy and Yang 2005).

Lignin is a highly cross-linked molecular complex with an amorphous structure and acts as “glue” between individual cells and between the fibrils forming the cell wall (Mohanty and others 2000). Lignin is first formed between neighboring cells in a “middle lamella,” bonding them tightly into a tissue, and then spreads into the cell wall penetrating the hemicelluloses and bonding the cellulose fibrils (Majumdar and Chanda 2001).

Chitosan is a heteropolysaccharide composed of β-1,4-linked 2-amino-2-deoxy-β-D-glucose obtained commercially by deacetylation of chitin, which is an abundant constituent of crustacean shells and fungi (Sebti and others 2005). Chitosan is considered a biocompatible, nonantigenic, nontoxic, and biofunctional fiber (No and others 2007). In addition, shrimp-derived chitosan was admitted as generally recognized as safe (GRAS) in 2005 by the USFDA (2007), based on scientific procedures for use in foods. Chitosan is not hydrolyzed specifically by digestive enzymes; however, there can be some digestion by bacterial flora and by nonspecific activity of some digestive enzymes such as amylases and lipases. Chitosan derivatives in the form of acetate, ascorbate, lactate, malate, and others are water-soluble (Borderías and others 2005).

Table 2 shows the content on total dietary fiber (TDF), soluble dietary fiber (SDF), and insoluble dietary fiber (IDF) of some cereals, vegetables, and fruits.

Table 2—.  Total dietary fiber, soluble dietary fiber, and insoluble dietary fiber of some cereals, fruits, and vegetables.
Food groupProductTotal dietary fiber (%)Total soluble dietary fiber (%)Total insoluble dietary fiber (%)Reference
CerealsWhole rye bread17.7012.70 5.00Hiller and others (2009)
Whole wheat17.00 2.3014.70Ragaee and others (2001)
Oat fiber97.00 4.0093.00Sabanis and others (2009)
Whole maize19.60 3.6016.0Picolli da Silva and Santorio-Ciocca (2005)
Fruits and vegetablesCitrus fiber71.62 9.2562.37Fernández-López and others (2009)
Carob fiber85.0011.0074.00Wang and others (2002)
Tiger nuts fiber59.71 0.10559.61Sánchez-Zapata and others (2009)
Guava fiber74.8024.7050.10Jiménez-Escrig and others (2001)
Cabbage fiber80.5017.6062.90Dongowski (2007)
Cocoa fiber60.5410.0950.45Lecumberri and others (2007)
Mango fiber28.0514.2513.80Vergara-Valencia and others (2007)
Apple fiber60.0015.0045.00Rosell and others (2009)
Sugar beet fiber76.9052.1024.80Dongowski (2007)
Carrot fiber80.7032.7048.00Kotcharian and others (2004)
Pea fiber86.70 6.9079.80Wang and others (2002)

Physiological Functionality of Fiber

Fiber as a reducing agent of hyperlipidemia and hypercholesterolemia

The beneficial effects of high-fiber diets in protecting against CVD are not limited to their effects on the risk of developing type 2 diabetes, or their contribution to weight loss. Evidence suggests that the increased consumption of insoluble as well as soluble dietary fibers can directly impact the risk of developing CVD by targeting risk factors such as elevated serum LDL-cholesterol levels (Chau and others 2004; Kendall and others 2009).The results from numerous epidemiological and clinical studies have been so convincing that moderate or higher intakes of dietary fibers can effectively lower CVD risk through its action on LDL-cholesterol (see Table 3). Generally, it has been demonstrated that a 1% reduction in serum levels of LDL-cholesterol corresponds to a 1% to 2% reduction in the occurrence of CVD events, making LDL-cholesterol an excellent intermediary biomarker for assessment of CVD risk (Kendall and others 2009).

Table 3—.  Overview of human clinical trials.
Clinical statusIngredientDose (g/d)Time (d)DecreaseReduction (%)Reference
Normal healthyHigh-fiber vegetable14014LDL-cholesterol33Jenkins and others (2001)
Normal healthyInulin1021Triglycerides16.3Letexier and others (2003)
Normal healthyInulin928Total cholesterol, triglycerides 7.9Brighenti and others (1999)
    21.2 
Normal healthyFOS9.421Total cholesterol, 4.4Schaafsma and others (1998)
   LDL-cholesterol, LDL/HDL 5.4 
     5.3 
Normal healthyPectins, gums, mucilages, hemicelullose, cellulose and lignins3090LDL-cholesterol12.8Aller and others (2004)
Normal healthyβ-Glucan377Total cholesterol, 4.5Karmally and others (2005)
   LDL-cholesterol, 5.3 
Normal healthyInulin1056Triglycerides18.9Jackson and others (1999)
Normal healthyBamboo fiber28 6Total cholesterol, 9.6Park and Jhon (2009)
   LDL-cholesterol, triglycerides15.3 
    12.7 
Mildly hypercholesterolemicβ-Glucan5.949LDL-cholesterol, LDL/HDL 6.7Kerckhoffs and others (2003)
     5.4 
Mildly hypercholesterolemicβ-Glucan635Total cholesterol,20.0Behall and others (2004)
   LDL-cholesterol, triglycerides24.0 
    16.0 
Mildly hypercholesterolemicβ-Glucan335Total cholesterol,17.0Behall and others (2004)
   LDL-cholesterol, triglycerides17.0 
    10.0 
Mildly hypercholesterolemicGuar gum, pectin, soy fiber and pea fiber2063Total cholesterol, 8.5Knopp and others (1999)
   LDL-cholesterol,12.1 
   LDL/HDL 9.4 
Mildly hypercholesterolemicCoconut fiber2514Total cholesterol,10.8Trinidad and others (2006)
   LDL-cholesterol, triglycerides 9.2 
    21.8 
Mildly hypercholesterolemicCoconut fiber1514Total cholesterol, 6.9Trinidad and others (2006)
   LDL-cholesterol, triglycerides11.0 
    19.3 
HypercholesterolemicCarob fiber1542LDL-cholesterol, triglycerides10.5Zunft and others (2003)
    11.3 
HypercholesterolemicPsyllium 5.1182Total cholesterol, 4.7Anderson and others (2000b)
   LDL-cholesterol, 6.7 
HypercholesterolemicGlucomannan 656Total cholesterol,18Martino and others (2005)
   LDL-cholesterol, triglycerides24 
    10 
HypercholesterolemicPsyllium10.256Total cholesterol,4Anderson and others (2000a)
   LDL-cholesterol,7 
HypercholesterolemicPolidextrose1526Total cholesterol, triglycerides 1.2Pronczuk and Hayes (2006)
    17.4 
HyperlipidemicInulin1842Total cholesterol, 1.3Davidson and others (1998)
   LDL-cholesterol, 2.1 
HyperlipidemicInulin728Total cholesterol, triglycerides21.5Balcazar-Muñoz and others (2003)
    27.3 
HyperlipidemicInulin2021Triglycerides14.0Causey and others (2000)
Hyperlipidemicβ-Glucan721LDL-cholesterol9.0Pomeroy and others (2001)
DiabeticsArtichoke fiber690Total cholesterol,4.54Nazni and others (2006)
   LDL-cholesterol, triglycerides11.37 
    10.37 

The exact mechanism by which dietary fibers lower serum LDL-cholesterol levels is not known. Evidence suggests that they may interfere with the lipid and/or bile acid metabolism. The hypocholesterolemic property of some dietary fiber, such as coconut is associated with the water-soluble fractions of fiber such as uronic acid, glucomannans, and galactomannans (Trinidad and others 2006). Uronic acid and galactomannans are not digested in the small intestine but are metabolized by the microflora in the large intestine and produce short-chain fatty acids such as acetate, propionate, and butyrate that contribute to lowering serum cholesterol levels: butyrate is primarily metabolized by colonic mucosal cells, while acetate and propionate are rapidly absorbed. It has been hypothesized that the production of short-chain fatty acids, and in particular changes in the propionate/acetate ratio, may influence lipid metabolism (Trinidad and others 2006; Theuwissen and Mensink 2008). Bean starches lower the levels of serum total cholesterol, VLDL-cholesterol, and LDL-cholesterol, increase the fecal concentration of short-chain fatty acids (in particular the butyric acid concentration), and increase fecal neutral sterol excretion (Martinez-Flores and others 2004).

Other suggested mechanisms include the inhibition of hepatic lipoprotein production and/or cholesterol synthesis by fermentation products and the delayed absorption of macronutrients leading to increased insulin sensitivity (Lunn and Buttriss 2007; Theuwissen and Mensink 2008). Mun and others (2005) reported that the reduction in the levels of cholesterol and other lipids by dietary fibers may be a consequence of an increase in aqueous phase viscosity, an alteration in droplet disruption or coalescence kinetics, and the reduced absorption of lipid, cholesterol, and bile acid.

For Lairon and others (2007) dietary fibers can affect lipid digestion or absorption in the small intestine through a variety of physicochemical mechanisms: (i) direct interaction with lipase: dietary fibers may interact directly with the lipase and/or co-lipase, thereby reducing their enzyme activity (Klinkesorn and McClements 2009); (ii) the formation of a protective membrane around lipid droplets: dietary fibers may adsorb around lipid droplets and form a protective coating that prevents the lipase/co-lipase from coming into close contact with the lipid substrate inside the droplets (Mun and others 2006); (iii) binding bile salts: some dietary fibers bind bile salts, which may prevent them from emulsifying the lipids in the small intestine or from transporting lipid digestion products from the droplets to the intestinal mucosa (Thongngam and McClements 2005); and (iv) viscosity enhancement: many dietary fibers increase the viscosity of the aqueous solution surrounding the lipid droplets, which may alter the efficiency of droplet disruption and coalescence in the stomach and small intestine (Gallaher and Schneeman 2003).

Some researchers suggest that fiber may increase the size of the circulating very-low-density lipoprotein cholesterol (VLDL) and chylomicrons with consequent increased exposure to lipoprotein lipolysis (Vahouny and Kritchevsky 1986). Glucomannan is a special hydrosoluble fiber with the same properties as insoluble fiber. It increases its original volume by about 100 times, after contact with water, which causes an increase in the volume and viscosity of gastrointestinal content and enhances intestinal transit. One consequence of this is the interference with food absorption (Trinidad and others 2006) (Figure 2a). The physical and chemical high-density structure of glucomannan may clarify its hypocholesterolemic activity. Chitosan is being used as a new source of dietary fiber because of its biocompatibility, low toxicity in animal organs, and its chemical structure which is similar to that of cellulose and is not cleaved by digestive enzymes in humans (Dutta and others 2009). It contains 1 amino group per residue, which produces high-positive-charge densities in acidic solutions, unlike other dietary fibers. Chitosan is considered a potential ingredient of functional foods because of its beneficial activity in lipid disorders (Koide 1998). Several studies have reported that chitosan has a hypocholesterolemic action in animal models and healthy humans (Liao and others 2007; Liu and others 2008; Zhang and others 2008). Chitosan acts as a weak anion exchange resin and exhibits substantial viscosity in vitro, either of which properties could mediate its hypocholesterolemic effect. Ausar and others (2003) propose that chitosan inhibits cholesterol absorption and increase bile acid excretion. Unlike fibers of vegetable origin, the amine groups of chitosan take one hydrogen ion from the acid fluids of the stomach, which causes the formation of a positively charged tertiary amine group. In this way, negatively charged molecules such as fats, fatty acids, other lipids, and biliary acids, interact with the chitosan (Borderías and others 2005). Chitosan also interferes by trapping neutral lipids such as cholesterol and other sterols by means of hydrophobic interactions. These electrostatic and hydrophobic bonds cause the formation of long polymeric compounds, which are weakly attacked by digestive processes in the organism. This mixture passes into the intestine, where the fat/chitosan emulsion immediately changes to an insoluble gel owing to the pH of the medium, and thus fat droplets cannot be attacked by pancreatic or intestinal enzymes (Ylitalo and others 2002).

Figure 2—.

Proposed action mechanisms of fiber to decrease the (re)absorption of cholesterol and bile acids. (a) Bolus; (b) cholesterol or bile acid binding; (c) thick layer.

Dietary fiber may influence bile acid metabolism. Bile acids are highly effective detergents that promote solubilization, digestion, and absorption of dietary lipids and lipid-soluble vitamins throughout the small intestine. High concentrations of bile salts are maintained in the duodenum, jejunum, and proximal ileum, where fat digestion and absorption take place (Ridlon and others 2006). Normally, they are almost completely reabsorbed in the ileum (Hofmann 1994). Several dietary fibers are able to interact with bile acids in the small intestine, resulting in a lower reabsorption, an increased transport toward the large intestine, and, finally, a higher excretion of bile acids (Dongowski and others 2003). Evidence suggests that some water-soluble fibers may form a thick unstirred water layer in the intestinal lumen. This layer may act as a physical barrier, thereby decreasing the (re)absorption of fats, including cholesterol and bile acids (Figure 2c). This would lead to an increased fecal output of these 2 components. Because the bile acid pool is limited, the higher excretion of bile acids requires an increased hepatic synthesis of bile acids. As a result, the hepatic conversion of cholesterol into bile acids increases, hepatic pools of free cholesterol decrease and, to reach a new steady-state, endogenous cholesterol synthesis increases. This is probably the major hypocholesterolemic pathway that occurs in hypercholesterolemic individuals or animals (García-Diez and others 1996; Theuwissen and Mensink 2008).

Another possible mechanism is a reduction in the absorption of lipid, cholesterol, and bile acids, which could alter micelle formation and decrease the ability of cholesterol to incorporate into micelles (Carr and Jesch 2006). Dietary fiber has the capacity to bind bile acids, metabolites of cholesterol which play an important role in the digestion and absorption of lipids in the small intestine (Figure 2b). A high bile acid binding ability of fiber could lead to lower serum cholesterol concentrations by interrupting enterohepatic circulation (Eastwood 1992). Eastwood and Morris (1992) reported that the primary attribute of soluble fibers that inhibit cholesterol absorption is their ability to form a viscous matrix when hydrated. Many water-soluble fibers become viscous in the small intestine. It is believed that increased viscosity impedes the movement of cholesterol, bile acids, and other lipids and hinders micelle formation, thus reducing cholesterol absorption and promoting cholesterol excretion from the body (Carr and Jesch 2006). Pectin, β-glucans, fructans, and gums have been identified as agents that can work through the production of a viscous matrix that hinders movement of cholesterol and bile acids into micelles as well as the subsequent uptake of micelles into the enterocyte (Jones 2008). If viscosity in the lumen of the gut is important for physiological efficacy, it is important to understand which factors in a food might reduce or enhance the ability of pectin or β-glucans to generate viscosity. In the most general sense, the manner in which a soluble fiber will modify solution properties depends on the amount, solubility, or extractability under physiological conditions and the molecular weight and structure of the fiber. Changes in these properties of pectin or β-glucans in a food product may profoundly influence the physiological response (Wood 2007). Some fibers, such as, oligofructose and inulin are not viscous fibers but rather serve as excellent fuel sources for beneficial intestinal bacteria, particularly Lacobacillus spp. and Bifidobacterium spp (Boeckner and others 2001). In this way, changes in intestinal microflora induced by oligofructose and inulin have been shown to alter the bile acid profile and promote fecal bile acid excretion (Trautwein and others 1998).

Cholesterol 7-α-hydroxylase is the key regulatory enzyme in the synthesis of bile acids. The primary bile acids (Figure 3), cholic acid (3α,7α,12α-trihydroxy-5β-cholan-24-oic acid) and chenodeoxycholic acid (3α,7α-dihydroxy-5β-cholan-24-oic acid), are dehydrolyzed and converted to secondary bile acids, called deoxycholic acid (3α,12α-dihydroxy-5β-cholan-24-oic acid) and lithocholic acid (3α-hydroxy-5β-cholan-24-oic acid), respectively (Rodríguez and others 2006). The activity of this important rate-determining enzyme, cholesterol 7-α-hydroxylase, has been observed to increase in a dose-dependent manner in fiber-supplemented diets (Buchman and others 2000). Intestinal bacteria are able to convert the primary bile acids into various types of secondary bile acids too (Ridlon and others 2006). Colonic bacteria also contribute to the recovery of bile salts that escape active transport in the distal ileum. The major bile salt modifications in the human large intestine include deconjugation, oxidation of hydroxy groups at C-3, C-7, and C-12, and 7α/β-dehydroxylation. The deconjugation and 7α/β-dehydroxylation of bile salts increases their hydrophobicity and their Pka, thereby permitting their recovery via passive absorption across the colonic epithelium (Ridlon and others 2006).

Figure 3—.

Other physiological effects of dietary fiber.

Naumann and others (2006) reported that a ß-glucan-enriched meal is thought to increase bile acid binding which, in turn, may (i) decrease reabsorption of bile acids and drive bile acid synthesis from hepatic cholesterol, hence depleting the body's cholesterol pool and/or (ii) decrease absorption of intestinal cholesterol. The degree of absorption of common bile acids, lithocholic, deoxycholic, chenodeoxycholic, and cholic acids and cholesterol by fiber from plant food depends on the kind of raw material, conditions of processing, and type of bile acid (Górecka and others 2002). Schwiggert and others (2009) reported that the bile acid binding capacity seems to depend on various properties of the plant cell wall material such as particle size, surface characteristics (hydrophobicity), and molecular structure. There are also effects of bile acid structure on the extent of the interactions with dietary fiber. Dihydroxy-bile acids, such as glycochenodeoxycholic acid and glycodeoxycholic acid were more strongly bound to dietary fiber preparations than were trihydroxy-bile acids (Drzikova and others 2005). Górecka and others (2005) reported that dihydroxy-bile acids such as deoxycholic acid are bound more strongly by cereal products than monohydroxy-bile acids, such as lithocholic acid or trihydroxy-bile acid (cholic acid). Fechner and others (2009) reported that Boregine fiber (Lupinus angustifolius boregine) significantly increased the daily excretion of cholic acid from 9 to 15 mg/d and chenodeoxycholic acid from 9 to 13 mg/d in the stool. Boregine, Typ Top (Lupinus albus), and soy (Glycine max hefeng) reduced the concentration of the total bile acids and secondary bile acids. Soy was the only fiber which also decreased the concentration of primary bile acids. In addition to plasma cholesterol, plasma triacylglycerol concentrations, and fatty acid synthesis, may be altered by ingestion of viscous fiber. Topping and others (1988) fed adult rats diets containing methylcellulose (80 g/kg) as the fiber source. The methylcellulose was obtained in 3 different viscosities: low (25 cP), medium (400 cP), and high (1500 cP). After 10 d, a 2.2-fold reduction in hepatic fatty acid synthesis was observed in the rats consuming the high-viscosity methylcellulose. In addition, plasma triacylglycerol concentrations were lower (P < 0.05) in rats consuming high-viscosity methylcellulose compared with low-viscosity methylcellulose (1.2 and 1.6 μmol/mL, respectively). Dongowski (2007) studied different types of commercial and laboratory-made dietary fibers. Digested cereal products (barley, oat, rye, and wheat flour; oat bran), alcohol-insoluble substances from apples, strawberries, rowan berries, carrots, white cabbage, red beets, and sugar beet pulp, as well as arabinoxylan, bind 1.21 to 1.77 μmol bile acids/100 mg, while Novelose™ (a commercial fiber) binds approximately 0.65 μmol bile acids/100 mg. Carob fiber had the highest binding capacity (1.83 to 1.96 μmol bile acids/100 mg) whereas cellulose had no effect. For Kahlon and Smith (2007) the variability in bile acid binding between the fruits tested may be related to their phytonutrients, antioxidants, polyphenols, flavonoids (anthocyanins, flavonols, and proanthocyanidins), structure, hydrophobicity of undigested fractions, and anionic or cationic nature of the metabolites produced during digestion or their interaction with active binding sites. These reearchers reported that bile acid binding, on a dry matter basis, of bananas (0.90 μmol bile acids/100 mg) was significantly higher than that of nectarines (0.21 μmol bile acids/100 mg) and significantly lower than those for peaches (0.60 μmol bile acids/100 mg), pineapple (0.59 μmol bile acids/100 mg), grapes (0.50 μmol bile acids/100 mg), pears (0.47 μmol bile acids/100 mg), and apricots (0.31 μmol bile acids/100 mg). Schwiggert and others (2009) investigated the bile acid binding capacity of the lupine fiber products with an in vitro assay. The lupine dietary fiber product showed a bile acid binding capacity of about 19% of that of the pharmaceutical cholestyramine (a cholesterol-lowering, bile acid–binding drug). Kahlon and Chow (2000) found that different cereal brans, β-glucan-enriched barley and ready-to-eat breakfast cereals bound 0.3 to 1.8 μmol bile acids/100 mg. Cholestyramine was the positive control treatment, and cellulose was the negative control. Kahlon and others (2007) reported that the in vitro bile acid binding, on a dry matter basis, of some vegetables (relative to cholestyramine) was: beets, 18%; okra, 16%; eggplant, 14%; asparagus, 10%; carrots, 8%; green beans, 7%; cauliflower, 6%; and turnips, 1%.

There is strong clinical evidence suggesting that the use of viscous fibers reduces serum cholesterol and the subsequent risk of CVD. This relationship is amplified when other cholesterol lowering foods are used alongside viscous fibers. Evidence on the possible role of whole grain fibers and CVD are less conclusive. While cohort studies suggest a protective role, clinical trials show a lack of metabolic benefit. Randomized trials need to be undertaken to strengthen the evidence on the possible relationship or the lack thereof (Kendall and others 2009).

Other Physiological Effects

Extracts rich in dietary fiber obtained from plants can be used as functional ingredients (Fernández-López and others 2007; Pérez-Alvarez 2008b; Sendra and others 2008) since the fibers may interact physiologically to provide numerous health benefits that go far beyond supporting bowel regularity. These benefits may include not only digestive health, but weight management, cardiovascular health, and also general wellness.

Indeed hyperlipidemia, and hypercholesterolemia effects, diets naturally high in dietary fiber, can be considered to bring about 4 main physiological consequences (Figure 4): (i) improvements in gastrointestinal health; (ii) improvements in glucose tolerance and the insulin response; (iii) reduction in the risk of developing some cancers; and (iv) lipid digestion and hence some degree of weight management (Lunn and Buttriss 2007).

Figure 4—.

Bile acids, classification, and chemical structure.

Improvements in gastrointestinal health

The fact that fiber can bind a large amount of water makes it highly useful from a physiological point of view, since it enlarges the volume of the aqueous phase of the food pellet and slows down the absorption of nutrients in the intestine (Gallaher and Schneeman 1986). It is now recognized that the traditional chemoprotective role of dietary fiber, which formerly consisted of fecal bulking, rapid transit, and augmenting the fecal volume and the frequency of evacuation, may have added benefits (Cummings 2001; Spiller and Spiller 2001). These purported health-promoting properties could include the so-called prebiotic activity (Gibson and Roberfroid 1995), putatively encompassing cell protective effects of particular antioxidants that can be liberated in the colon after fermentation by the gut flora (Ferguson and others 2005).

The type, source, and amount of the fiber influence the intestinal function in different ways; in general, fibers that are resistant to colonic fermentation, such as wheat bran, mostly increase the content of the intestine. However, highly fermentable fibers generate a large mass of microorganisms and thus, likewise, increase the intestinal content (Borderías and others 2005).

Improvements in glucose tolerance and the insulin response

The beneficial effect of dietary fiber on postprandial metabolic parameters and glucose control has been the object of many studies over recent decades (Kabir and others 2002; Behall and others 2006). Several studies have shown that the risk of type 2 diabetes mellitus is inversely correlated with the intake of diets with a low glycemic index or with high fiber content (Schulze and others 2004). Reductions in plasma glucose concentrations, as a result of the consumption of viscous fiber sources may be due to several events. First, ingested viscous fibers cause slow gastric emptying by forming a gel matrix as a result of their water-holding capacity (Wursch and Pi-Sunyer 1997). As these hydrated fibers enter the small intestine, the gel matrix may thicken the small intestinal contents, modulating digestive processes by decreasing the diffusion of nutrients for absorption, and contact between food and digestive enzymes. In addition, viscous fibers could alter the resistance of contractile movements within the gastrointestinal tract and thereby decrease the transport of glucose to absorptive surfaces. Furthermore, at the absorptive surfaces, the ingestion of viscous fibers may thicken the unstirred water layer through which glucose and cholesterol diffuse very slowly (Edwards and others 1988; Mälkki 2001).

Reduction in the risk of developing some cancers

Fiber and starch are thought to be important protective factors, with a strong inverse relationship between starch consumption and colorectal cancer incidence (Topping and others 2008). Several mechanisms that might explain the protective effect of fiber have been proposed.

Soluble fiber has a positive impact on colonic health by increasing the crypt cell production rate, or decreasing colonic epithelial atrophy in comparison with nonfiber diets (Slavin and others 2009). Dietary fiber might reduce the risk of colorectal cancer by increasing the speed of transit of food material through the large intestine, by fermentation in the large bowel, and by producing high levels of short-chain fatty acids (Sharma and others 2008). The butyric acid or its salts may promote cell differentiation, induce apoptosis, and/or inhibit the production of secondary bile acids by reducing luminal pH (Nagengast and others 1995; Potter 1999). There is evidence that butyrate may reduce the risk of malignant changes in cells. Population studies in the cecum of rats fed with dietary fiber preparations have shown that increase in fecal bulking and lower fecal pH, as well as greater production of SCFA, is associated with the decreased incidence of colon cancer, which have been suggested to resemble the effects of soluble dietary fiber (Tharanathan and Mahadevamma 2003).

Lipid digestion and some degree of weight management

Dietary fiber intake seems to best predict total energy intake, with several reports of lower total energy intake with high-fiber as compared to low-fiber diets (Pereira and Ludwig 2001). Keenan and others (2006) reported that the use of resistant starch in the diet as a bioactive functional food component is a natural, endogenous way to increase gut hormones that are effective in reducing energy intake, so may be an effective natural approach to the treatment of obesity. A number of researchers have examined the potential of dietary fiber to modify fat oxidation and various studies have examined its potential as a satiety agent and also a contributar to weight management (Sharma and others 2008; Mikušová and others 2009), although the results are still not conclusive. It is proposed that eating a diet rich in fiber may increase the mobilization and use of fat stores as a direct result of a reduction in insulin secretion (Tapsell 2004). There are probably several reasons why high-fiber diets are associated with lower food intake. First, high-fiber diets may trigger maximal sensory stimulation in the mouth due to the increased need for chewing. High-fiber diets also lead to slower gastric emptying and a slower rate of nutrient absorption. Finally, a high-fiber diet reduces the energy density of the overall diet. Regardless of the reason, increasing dietary fiber is generally thought to aid in weight management (Hill and Peters 2002).

Technological Functionality

The functional properties of plant fiber depend on the IDF/SDF ratio, particle size, extraction condition, and vegetable source (Jaime and others 2002). From a technological point of view, dynamic viscosity, gelling ability, hydration properties, and viscous and elastic characteristics of soluble and insoluble dietary fiber have proven to account for major properties with variable influence on the functionality of fiber-supplemented foods (Collar and Angioloni 2009).

The physiological functions of the DF are often attributed to its physicochemical properties, water-holding capacity, swelling, rheological, and fat binding properties, and susceptibility to bacterial degradation or fermentation (Dikeman and Fahey 2006).

The dietary fibers from cereals are more frequently used than those from fruits; however, fruit fibers have, in general, better nutritional quality than those found in cereals, because of their significant contents of associated bioactive compounds (flavonoids, carotenoids, and others) and more balanced composition (higher overall fiber content, greater SDF/IDF ratio, water- and fat-holding capacities, lower metabolic energy value, colonic fermentability, as well as lower phytic acid content (Chau and Huang 2003; Figuerola and others 2005).

Water holding capacity (WHC)

The most important property from a technological standpoint is the ability to bind water. WHC depends on several factors such as:

  • (i) Particle size: Sangnark and Noomhorm (2003) reported that a decrease in fiber particle size was associated with a reduction in water holding capacity.
  • (ii) Processing: washing increases WHC probably because of removal of sugars (Larrauri 1999).
  • (iii) Type of fiber: Soluble fibers possess a higher WHC than insoluble fibers (Rosell and others 2009).

Oil holding capacity (OHC)

OHC, also, is an important property. It represents the capacity of a fiber to bind fat, and depends on:

  • Porosity: The porosity of the fiber is more important than molecular affinity to bind the fat (Nelson 2001).

  • Particle size: the lower the particle size, the higher the oil holding capacity.

Washing does not affect the OHC (Lario and others 2004).

Chelating capacity

The chelating properties of DF depend on the chemical structure and mass fraction of the components. Thus, hemicellulose and pectins are among those with a remarkable ability to bind heavy metals (Nawirska and Kwasniewska 2005). The chelating capacity of the preparations has been found to be influenced by DF origin (fractional composition), experimental conditions (pH, temperature), and the type of the metal being investigated (Nawirska and Oszmianski 2001).

Gel-forming capacity

Gel is the name given to an association of polymeric units to form a network in which water and/or other solutes are included. Many soluble fibers form gels, for instance, carrageenans, pectins, konjac, and so on. The capacity to form a gel and the characteristics of that gel will depend on a number of factors including concentration, temperature, presence of certain ions, and pH (Borderías and others 2005).

Fermentative capacity

Fibers are able to ferment to various extents depending on the type of fiber. Thus, whereas cellulose ferments to a very small extent, pectins are entirely fermentable (Gallaher and Schneeman 2003).

The ideal dietary fiber should meet the following requirements (Saura-Calixto and Larrauri 1996):

  • (i) Have no nutritionally objectionable components.
  • (ii) Be as concentrated as possible so that minimum amounts can have a maximum physiological effect.
  • (iii) Be bland in taste, color, texture and odor.
  • (iv) Have a balanced composition (insoluble and soluble fractions) and adequate amounts of associated bioactive compounds.
  • (v) Have a good shelf life that does not adversely affect that of the food to be formulated.
  • (vi) Be compatible with food processing.
  • (vii) Have the right, positive image in the eyes of the consumer with regard to source, wholesomeness, and so on.
  • (viii) Have the expected physiological effects.
  • (ix) Be reasonable in price.

Foods Enriched with Dietary Fiber

The importance of food fibers has led to the development of a large potential market for fiber-rich products and ingredients and, in recent years, there has been a trend to find new sources of dietary fiber that can be used as ingredients in the food industry (Chau and Huang 2003). At present, a great variety of foods, including meat products (Alesón-Carbonell and others 2005; Fernández-López and others 2007; Fernández-López and others 2008), fish (Sánchez-Zapata and others 2008), breakfast cereals and bakery products (Vergara-Valencia and others 2007), and dairy products (García-Pérez and others 2006; Sendra and others 2008) have been enriched with fiber (Figure 5). Table 4 lists how certain types of fiber have been used, for different purposes, in foods.

Figure 5—.

Foods enriched with dietary fiber.

Table 4—.  Food products enriched with different types of fiber.
Food groupFoodType of fiberTechnological effectReference
Bakery productsBread and cookiesMango dietary fiberAnti-radical efficiencyVergara-Valencia and others (2007)
CookiesApple and lemon fiberLower phytic acid contentsBilgiçli and others (2007)
BreadCarob and pea fiberSofter crumbsWang and others (2002)
CookiesSugarbeet fiberIncreased the total dietary fiberOzturk and others (2008)
Wire-cut cookiesLemon fiberHarder samplesUysal and others (2007)
FlakesCoconut fiberIncreased the total dietary fiber contentTrinidad and others (2006)
BiscuitsMango fiberImproved antioxidant propertiesAjila and others (2008)
CakeNopal fiberIncreased overall acceptabilityAyadi and others (2009)
BreadLupin kernel fiberBeneficial effects on blood glucose and insulin measuresJohnson and others (2003)
BreadWheat fiberLower postprandial glucose concentrationsFeldheim and Wisker (2002)
Meat productsMeat battersRice bran fiberRegular fat controlChoi and others (2009)
Beef frankfurtersSugarbeet fiberIncreased total dietary fiber content and water-holding capacityVural and others (2004)
MeatballsOat branHigh acceptabilityYılmaz and Daglıoglu (2003)
Cooked-meat sausageOrange fiberHypocaloric productGarcía and others (2007)
Dry-cured sausageOrange fiberReduction in residual nitrite levelsFernández-López and others (2008)
Bologna sausageOrange fiberIncreased antioxidant activityViuda-Martos and others (2008)
Dry-cured sausageOrange fiberBetter organoleptic characteristicsGarcía and others (2002)
Bologna sausageLemon albedoReduction in residual nitrite levelsFernández-Ginés and others (2004)
Breakfast sausageCitrus fiberIncreased antioxidant activityAlesón-Carbonell and others (2005)
Dairy productsFermented milkCitrus fiberIncreased textural propertiesSendra and others (2008)
YogurtWheat and apple fiberDecreased availabilities of both calcium and glucoseRodríguez and others (2008)
Petit-suisse cheeseInulinImprove sensory qualityCardarelli and others (2008)
White-brined cheeseOat fiberIncreased textural propertiesVolikakis and others (2004)
YogurtAsparagus fiberIncreased sensory acceptance.Sanz and others (2008)
Fermented milkChicory inulinIncreased viability of bifidobacteriaVarga and others (2006)
Yogurt cheeseInulinIncreased survival of probiotic bacteriaSalem and others (2007)
YogurtWheat and apple fiberIncreased sensory acceptanceStaffolo and others (2004)
Fish productsRestructured hake productsChicory fiberIncreased hardnessCardoso and others (2007)
Restructured fish productsWhite grape fiberIncreased antioxidant activitySánchez-Alonso and others (2008)
SurimiChitosanIncreased the breaking force and deformation of gelsBenjakul and others (2001)
Tuna “pate”Citrus fiberIncreased antioxidant activitySánchez-Zapata and Pérez-Alvarez (2008), Sánchez-Zapata and others (2008b)
Cod sausageChitosanIncreased elasticityLópez-Caballero and others (2005)
Fish sausagePea fiberLower fat contentCardoso and others (2008)
Restructured fish productsWheat fiberIncreased the water holding capacitySánchez-Alonso and others (2007)

The enrichment of bakery products has traditionally consisted of the addition of unrefined cereals; however, there is a trend towards using other DF sources, mainly fruits, which present better nutritional quality, higher amounts of total and soluble fiber, a lower caloric content, stronger antioxidant capacity, and greater degrees of fermentability and water retention (Wang and others 2002; Nazni and others 2006; Uysal and others 2007; Vergara-Valencia and others 2007; Ozturk and others 2008).

In the case of meat or fish products, the addition of dietary fiber affects the physicochemical properties of the product including a reduction in the residual nitrite levels (Fernández-Ginés and others 2004; Fernández-López and others 2008) or increased antioxidant activity (Alesón-Carbonell and others 2005; Sánchez-Alonso and others 2008; Sánchez-Zapata and Pérez-Alvarez 2008; Viuda-Martos and others 2008) due to their significant content of associated bioactive compounds, such as phenolic acids, flavonoids, carotenoids, and so on (Fernández-López and others 2009). Dietary fiber can be used, too, for improving the organoleptic characteristics of meat products such as dry-cured sausages or meatballs (García and others 2002; Yılmaz and Daglıoglu 2003). They have the ability to increase the water retention capacity, while their inclusion in the meat matrix contributes to maintaining its juiciness, which means that the volatile compounds responsible for the flavor of the product are released more slowly (Chevance and others 2000).

Some types of fiber, as those from cereals or fruits, are used as functional ingredients in dairy products to improve the textural properties, the flavor properties, and the viability of probiotic bacteria (Staffolo and others 2004; Volikakis and others 2004; Varga and others 2006; Salem and others 2007; Cardarelli and others 2008; Sanz and others 2008; Sendra and others 2008).

In the case of beverages and drinks, the addition of DF increases their viscosity and stability, soluble fiber being the most used because it is more dispersible in water than insoluble fiber. Some examples of these soluble fibers are pectins (Mirhosseini and others 2008; Sampedro and others 2008), ß-glucans (Naumann and others 2006; Juvonen and others 2009), and gums (Bénech 2008; Yadav and others 2009).

Conclusions

Fiber consumption has been reduced significantly in western society and is far below the recommended level. The main reason has been the change in life style, which has promoted a significant reduction in fruit, vegetables, and legume consumption. With the aim of increasing fiber intake in the diet, many fiber-enriched foods have been developed. The addition of fibers to food products is of great interest not only as a means of improving the functionality of food products, but also as a means to create functional foods with health benefits. Given the remarkable range of benefits ascribed to dietary fiber there is clearly a need for an agreed-upon definition, which can be used for food labeling, setting nutrient reference values, and determining appropriate analytical methods and decisions relating to health claims.

To improve our knowledge of dietary fiber composition and structure, together with our understanding of its physiological effects on the human body, collaborative studies are needed involving the participation of researchers from different scientific areas: chemistry, biochemistry, biotechnology, biology, physiology, nutrition, and medicine.

Ancillary