Abstract
In the current context from the nutritional and epidemiological point of view, it can be seen an occurrence increase of Chronic Non-Communicable Diseases, as well as the inflammatory ones, ordinarily associated to a wrong feed, poor in fibers and rich in fats and simple and refined carbohydrates. This view has evidenced a progressive increase of diseases, highlighting the importance of colonic microbiota as an active mechanism of infectious processes control and modulation of immunologic answer. Therefore, constant the worries related to recovering and maintenance of healthy intestines, stocked with prebiotic nutrients that support the survival of beneficial health agents. This way, researchers and the segment of food industry has encouraged the development of products with prebiotic properties, looking for the health promotion, treatment and diseases prevention, besides the strengthening on the competitive market. This article will embrace the contents about physiologic effects of the main known prebiotic, their potential in relation to fermentatives bacterias, new developed products and used methodologies to the recognition of pre and probiotic functions.
prebiotics; physiologic effect; functional foods market
1 Introduction
Production of functional foods containing prebiotic ingredients, is an area that has
dominant featuring in the food industry in recent years, and a very promising
market, not only for economic reasons but by scientific evidence of its benefits.
Consumers are more aware the relationship between good nutrition and increasingly
seek for food that in addition to nurture, provide health benefits (Burgain et al., 2011Burgain, J., Gaiani, C., Linder, M., & Scher, J. (2011).
Encapsulation of probiotic living cells: From laboratory scale to industrial
applications. Journal of Food Engineering, 104(4), 467-483.
http://dx.doi.org/10.1016/j.jfoodeng.2010.12.031.
http://dx.doi.org/10.1016/j.jfoodeng.201...
). Aiming to satisfy this
new market, some prebiotics, especially inulin and fructooligosaccharide, have been
incorporated into a wide variety of foods and beverages that are part of a natural
diet as dairy products, breads, cereals, dietary supplements, and others. Through
this growth consumers can appreciate tasty meals while promoting beneficial effects
to their own health (Coman et al.,
2012Coman, M. M., Cecchini, C., Verdenelli, M. C., Silvi, S., Orpianesi,
C., & Cresci, A. (2012). Functional foods as carriers for SYNBIO®, a
probiotic bacteria combination. International Journal of Food Microbiology,
157(3), 346-352. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.06.003.
PMid:22727086
http://dx.doi.org/10.1016/j.ijfoodmicro....
).
Prebiotics exert a myriad of effects of health promotion, a fact that has attracted
an ever growing number of food processing and pharmaceutical industries. Prebiotics
are involved in formulating starter culture, maintaining intestinal health,
inhibiting cancer, prevention of obesity and constipation. They also seem to promote
a positive modulation of the immune system (Delgado
et al., 2011Delgado, G. T. C., Tamashiro, W. M. S. C., Maróstica Junior, M. R.,
Moreno, Y. M. F., & Pastore, G. M. (2011). The putative effects of
prebiotics as immunomodulatory agents. Food Research International, 44(10),
3167-3173. http://dx.doi.org/10.1016/j.foodres.2011.07.032.
http://dx.doi.org/10.1016/j.foodres.2011...
). Recent trends about innovative sources of food waste,
supplementation of prebiotics in the diet, evaluation to biotechnological synthesis
of prebiotics. Researchers around the world are looking for alternatives to improve
access to these ingredients, so they start to be known and consumed by the
population in general.
This article reviews some of the physiological effects of prebiotic ingredients and developing products, highlighting its potential health and positive perspective for consolidation in the functional foods market.
2 Methodology
This article consists of a literature review, in which matters are related to the physiological effects and beneficial to health, characteristics and food applications of prebiotic ingredients. Was used as a source of research, scientific databases, if opting for articles published in the last 15 years, in Portuguese, English and Spanish.
3 Prebiotic physiologic effects
Knowledge of prebiotic as dietetics modular to the intestinal microbiota was sourced by the authors Gibson & Roberfroid (1995)Gibson, G. R., & Roberfroid, M. B. (1995). Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. The Journal of Nutrition, 125(6), 1401-1412. PMid:7782892. when defined prebiotic as a feeding ingredient resistant to digestion, that has beneficial effects because it is able to selectively stimulate the growth and/or activity of a limited number of bacteria in the colon, when suffering fermentation, getting this way a primary role in the intestinal physiology.
Besides guaranteeing healthy intestines, prebiotics are admittedly important thanks
to many facts, as: due to the bioprocess, they produce microbian biomass, increasing
the number of defecations, having, this way similar function to the feeding fibers
(Mann et al., 2007Mann, J., Cummings, J. H., Englyst, H. N., Key, T., Liu, S.,
Riccardi, G., Summerbell, C., Uauy, R., van Dam, R. M., Venn, B., Vorster, H.
H., & Wiseman, M. (2007). FAO/WHO scientific update on carbohydrates in
human nutrition: conclusions. European Journal of Clinical Nutrition, 61(Suppl.
1), S132-S137. http://dx.doi.org/10.1038/sj.ejcn.1602943.
PMid:17992184
http://dx.doi.org/10.1038/sj.ejcn.160294...
); They serve as an
alternative food to the probiotics, because they inhibit the pathogens
multiplication; They prevent diarrhea situations and other diseases like colon
cancer; They establish favorable mechanisms to imunomodulation; They act in the
absorption of calcium and also in lipid metabolism; They act as functional
ingredients as sugar and fat substitutes, besides promoting the best sensorial
characteristics in food.
Main prebiotic actors are fructan inulin and fructooligossacharides (FOS), no structural polysaccharides in major occurrence among plants, after starch and saccharose. They are considered carbohydrates of reservation, of linear or branched chain, existent in various vegetables species, like onion, celery, asparagus, Jerusalem artichokes, chicory roots, yacon potato, among many others (Quinteros, 2000Quinteros, E. T. T. (2000). Produção com tratamento enzimático e avaliação do suco de yacon (Tese de Doutorado). Faculdade de Engenharia de Alimentos, Universidade Estadual de Campinas, Campinas.).
Inulin has linear chain united by links β(2-1), important by being resistant to
enzymatic hydrolysis of human gastrointestinal, and degree of polymerization from 11
to 65 units of fructose with a terminal glucose. Since inulin hydrolysis FOS chains
are formed, containing from 2 to 10 units of fructose (Roberfroid, 2005Roberfroid, M. B. (2005). Introducing inulin-type fructans. The
British Journal of Nutrition, 93(Suppl. 1), S13-S25.
http://dx.doi.org/10.1079/BJN20041350. PMid:15877886
http://dx.doi.org/10.1079/BJN20041350...
). Fructan are bifidogenic and not dependent
of the size of the chain and the presence or absence of glucose in their
composition. It is necessary to highlight inulin because of its major polymerization
degree ferments FOS, getting maximum fermentation in the peripheral colon (Lajolo & Menezes, 2006Lajolo, F. M., & Menezes, E. W. (2006). Carbohidratos en
alimentos regionales Iberoamericanos. São Paulo: Universidade de São
Paulo.).
When fructan get to the large intestines they are totally fermented by bacteria that
live in the intestines. Colon contain a complex and dynamic microbial ecosystem,
with big concentration of bacteria coming up to more than 1011 to
1012 units that form colonies for milliliters (UFCmL–1)
(Berg, 1996Berg, R. D. (1996). The indigenous gastrointestinal microflora.
Trends in Microbiology, 4(11), 430-435.
http://dx.doi.org/10.1016/0966-842X(96)10057-3. PMid:8950812
http://dx.doi.org/10.1016/0966-842X(96)1...
). A major part of
intestinals bacteria is beneficial; however, some species are pathogenic and may be
enrolled in the acute or chronic disease development. Considered no pathogenic or
beneficial bacteria, bifidobacterium and lactobacilli has positive biologic
activities in human health and are common aims of dietetics interventions (Cummings & Macfarlane, 2002Cummings, J. H., & Macfarlane, G. T. (2002). Gastrointestinal
effects of prebiotics. The British Journal of Nutrition, 87(Suppl. 2),
S145-S151. http://dx.doi.org/10.1079/BJN/2002530. PMid:12088511
http://dx.doi.org/10.1079/BJN/2002530...
).
Lactobacilli species are widely studied due to their properties that stimulate health. They have an important commercial value to food industry, due to its appliance in milk derivate production and as beginning cultures of fermentation, commonly associated to bread fermentation (Buriti & Saad, 2007Buriti, F. C. A., & Saad, S. M. I. (2007). Bactérias do grupo Lactobacillus casei: caracterização, viabilidade como probióticos em alimentos e sua importância para a saúde humana. Archivos Latinoamericanos de Nutrición, 57(4), 373-380. PMid:18524322.).
Bifidobacteria makes the biggest group on the colon, the one that constitutes more
than 25% of the total of adult intestinal population and 95% in newborn, promote
diverse beneficial effects to the hostess, so as the substratum fermentation having
as a final result the production of short-chain fatty acids (SCFA), they are
acetate, propionate and butyrate. Beside this SCFA also formed lactate, bacterial
biomass and other gases (CO2, H2, and methane) (Cherbut, 2002Cherbut, C. (2002). Inulin and oligofructose in the dietary fibre
concept. The British Journal of Nutrition, 87(Suppl. 2), S159-S162.
http://dx.doi.org/10.1079/BJN2002532. PMid:12088513
http://dx.doi.org/10.1079/BJN2002532...
). Butyrate is considered the
main resource of energy to colonocytes, acetate and propionate walk around the
portal veins and can influence in the metabolism of carbohydrate and lipids (Silveira Rodríguez et al., 2003Silveira Rodríguez, M. B., Monereo Megías, S., & Molina Baena,
B. (2003). Alimentos funcionales y nutrición óptima. Cerca o lejos? Revista
Espanola de Salud Publica, 77(3), 317-331.
http://dx.doi.org/10.1590/S1135-57272003000300003.
PMid:12852326
http://dx.doi.org/10.1590/S1135-57272003...
).
Production of SCFA promotes reduction of pH that makes a bactericidal action,
reduction of serum levels of ammonia by the fermentation of proteins; production of
complex B vitamins, increase of mineral absorption, as calcium and magnesium and the
improvement of immune answer. Propionate participates of lipid metabolism
regulation, because it decreases the liver cholesterol synthesis by the inhibition
of hydroxymetylglutaryl coenzyme activity and participation on the regulation of
glucose metabolism, promoting the decrease of prandial and insulin answer (Perrin et al., 2002Perrin, S., Fougnies, C., Grill, J. P., Jacobs, H., & Schneider,
F. (2002). Fermentation of chicory fructo-oligosaccharides in mixtures of
different degrees of polymerization by three strains of bifidobacteria. Canadian
Journal of Microbiology, 48(8), 759-763. http://dx.doi.org/10.1139/w02-065.
PMid:12381033
http://dx.doi.org/10.1139/w02-065...
).
Among the most important functions of intestinal microbiotic is its capacity of inhibit the implementation of pathogenic or no pathogenic invaders microorganism, in the mucosa surface acts as a barrier against infections. It also helps in the selective transportation of nutrients, in the stimulus of the immunological system and in the toxins neutralization. Besides that, it participates in the medicine mechanism, cholesterol, in degradation of biliary salt and in the regulation of the urea cycle (Priebe et al., 2002Priebe, M. G., Vonk, R. J., Sun, X., He, T., Harmsen, H. J., & Welling, G. W. (2002). The physiology of colonic metabolism. Possibilities for interventions with pre- and probiotics. European Journal of Nutrition, 41(Suppl. 1), I2-I10. PMid:12420110.).
Countless factors can influence the type and extension of fermentation of determined
substrates. It includes the competition for nutrients, characteristics of
microbiotica colonic, the hostess conditions, interaction among bacteria and the
individual feeding habits. Biomass and production of lactate and acetate are higher
when the substrate contain more fructooligossacharides from a short chain (Perrin et al., 2002Perrin, S., Fougnies, C., Grill, J. P., Jacobs, H., & Schneider,
F. (2002). Fermentation of chicory fructo-oligosaccharides in mixtures of
different degrees of polymerization by three strains of bifidobacteria. Canadian
Journal of Microbiology, 48(8), 759-763. http://dx.doi.org/10.1139/w02-065.
PMid:12381033
http://dx.doi.org/10.1139/w02-065...
).
Bifidogenic effect in inulin has been evidenced in many scientific researches. Menne et al. (2000)Menne, E., Guggenbuhl, N., & Roberfroid, M. (2000). Fn-type chicory inulin hydrolysate has a prebiotic effect in humans. The Journal of Nutrition, 130(5), 1197-1199. PMid:10801918. also studied the prebiotic effect of inulin in humans, and verified positive modifications in the fecal microbiota composition, especially by the effect of bifidobacteria increase. Rafter et al. (2007)Rafter, J., Bennett, M., Caderni, G., Clune, Y., Hughes, R., Karlsson, P. C., Klinder, A., O’Riordan, M., O’Sullivan, G. C., Pool-Zobel, B., Rechkemmer, G., Roller, M., Rowland, I., Salvadori, M., Thijs, H., Van Loo, J., Watzl, B., & Collins, J. K. (2007). Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. The American Journal of Clinical Nutrition, 85(2), 488-496. PMid:17284748. studying patients with colon cancer verified that a symbiotic diet, using inulin, bifidobacteria and lactobacilli, resulted in meaningful increase of fecal microbiota with bifid and lactobacilli, and decrease of Clostridium perfringens.
Nowadays one of the ways of increase the number of beneficial intestinal microorganisms is the use of prebiotic ingredients and to be able to generate the bifidogenic effect is necessary that the counting of cultures prebiotics in the colon be higher or equal to 106 UFCg–1 of fecal material (Gibson & Fuller, 2000Gibson, G. R., & Fuller, R. (2000). Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. The Journal of Nutrition, 130(Suppl. 2), 391S-395S. PMid:10721913.).
On the other hand, Passariello et al. (2011)Passariello, A., Terrin, G., De Marco, G., Cecere, G., Ruotolo, S.,
Marino, A., Cosenza, L., Tardi, M., Nocerino, R., & Berni Canani, R. (2011).
Efficacy of a new hypotonic oral rehydration solution containing zinc and
prebiotics in the treatment of childhood acute diarrhea: a randomized controlled
trial. The Journal of Pediatrics, 158(2), 288-92.e1.
http://dx.doi.org/10.1016/j.jpeds.2010.07.055. PMid:20828714
http://dx.doi.org/10.1016/j.jpeds.2010.0...
,
evaluated the efficacy of zinc and prebiotics for treatment of diarrhea in children.
Result of the randomized controlled trial showed that the zinc and the prebiotics
limit diarrhea duration in patients by stimulating water and electrolyte absorption
across gut mucosa and inhibiting the pathogens, respectively. Therapeutic efficacy
was attributed to the synergistic relation between the additives.
4 Immunomodulatory effect
Although the genetic to be the main factor determining the intestinal flora has a
important role in the development of the defense system of the intestinal mucosa and
it is believed that many intestinal diseases are related to this immune regulation.
The oligosaccharides associated with intestinal bacteria guide the T lymphocytes
maturation, closely linked to the prevention of gastrointestinal diseases. This fact
is highlighted especially in infants, which will contribute to their future health
(Thomas et al., 2010Thomas, D. W., Greer, F. R., American Academy of Pediatrics
Committee on Nutrition, & American Academy of Pediatrics Section on
Gastroenterology, Hepatology, and Nutrition (2010). Probiotics and prebiotics in
pediatrics. Pediatrics, 126(6), 1217-1231.
http://dx.doi.org/10.1542/peds.2010-2548. PMid:21115585
http://dx.doi.org/10.1542/peds.2010-2548...
).
Some experts have seen a progressive increase on immune-mediated and gut physiology health problems, such as allergies and auto-immune and inflammatory diseases. In this context, the increased use of prebiotic fibres has become a major area of interest within the nutrition researchers. Some mechanisms contributing to altered in vivo immune function induced by functional foods may include modulation of the microflora itself, improved barrier function and direct effects of bacteria on different epithelial and immune cell types, like a monocytes, macrophages, B cells, T cells and NK cells (Romeo et al., 2010Romeo, J., Nova, E., Wärnberg, J., Gómez-Martínez, S., Díaz Ligia, L. E., & Marcos, A. (2010). Immunomodulatory effect of fibres, probiotics and synbiotics in different life-stages. Nutrición Hospitalaria, 25(3), 341-349. PMid:20593114.).
Studies reporting effects on immunity with prebiotics, for example in double-blind
design, randomised intervention study for 6 weeks with 38 infants, administered
doses of galacto-oligosaccharides (GOS) and fructo-oligosaccharides with 4,5g/day
and found the level of bifidobacteria in the intestinal microbiota increased (Scholtens et al., 2006Scholtens, P. A., Alles, M. S., Bindels, J. G., van der Linde, E.
G., Tolboom, J. J., & Knol, J. (2006). Bifidogenic effects of solid weaning
foods with added prebiotic oligosaccharides: a randomised controlled clinical
trial. Journal of Pediatric Gastroenterology and Nutrition, 42(5), 553-559.
http://dx.doi.org/10.1097/01.mpg.0000221887.28877.c7.
PMid:16707980
http://dx.doi.org/10.1097/01.mpg.0000221...
). Study for 12 weeks
with 74 elderly subjects found decreased levels of pro-inflammatory gene
transcription activation with 1,3g/day of oligosaccharides (Vulevic et al., 2008Vulevic, J., Drakoularakou, A., Yaqoob, P., Tzortzis, G., &
Gibson, G. R. (2008). Modulation of the fecal microflora profile and immune
function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy
elderly volunteers. The American Journal of Clinical Nutrition, 88(5),
1438-1446. PMid:18996881.). In a multicenter study with 342 healthy
infants using 0,4g/100ml/day of GOS/FOS found reduced intestinal and respiratory
infections during the first year of life (Bruzzese
et al., 2009Bruzzese, E., Volpicelli, M., Squeglia, V., Bruzzese, D., Salvini,
F., Bisceglia, M., Lionetti, P., Cinquetti, M., Iacono, G., Amarri, S., &
Guarino, A. (2009). A formula containing galacto- and fructo-oligosaccharides
prevents intestinal and extra-intestinal infections: an observational study.
Clinical Nutrition (Edinburgh, Scotland), 28(2), 156-161.
http://dx.doi.org/10.1016/j.clnu.2009.01.008. PMid:19231042
http://dx.doi.org/10.1016/j.clnu.2009.01...
).
Prebiotics have been extensively studied, hereby, they may become an ideal treatment
or co-treatment in inflammatory bowel disease, due their capacity to increase
endogenous lactobacilli and bifidobacterium. Advances in pathogenesis of intestinal
inflammation, suggesting prebiotics should be useful in this disorders. The use of
prebiotics as inulin and FOS, has led to decreased chronic inflammatory enteropathy
of the mouse and is associated with downregulation of the production of IL-6 and
IFN-gamma in the colonic samples (Peña,
2007Peña, A. S. (2007). Flora intestinal, probióticos, prebióticos,
simbióticos y alimentos novedosos. Revista Espanola de Enfermedades Digestivas,
99(11), 653-658. http://dx.doi.org/10.4321/S1130-01082007001100006.
PMid:18271664
http://dx.doi.org/10.4321/S1130-01082007...
).
5 Performance of prebiotics on the calcium and iron bioavailability
Some metabolic factors have been associated with prebiotics in relation to absorption of micronutrients such as calcium and iron, however, it is known that more research is needed to support these findings. There have been few randomized controlled studies with small numbers of subjects who have evaluated the absorption of calcium after the administration of prebiotics (FOS, GOS, inulin or combinations). Study randomized with subjects was shown that inulin administered over a year, not only improved calcium absorption but also the bone mineral density per year (Olveira Fuster & González-Molero, 2007Olveira Fuster, G., & González-Molero, I. (2007). Probióticos y prebióticos en la práctica clínica. Nutrición Hospitalaria, 22(Suppl 2), 26-34. PMid:17679291.).
Yacon (Smallanthus sonchifolius) roots have been considered a
functional food due to the high levels of fructans they contain. Another study
evaluated Ca and Mg balance, bone mass and strength, and caecum mucosal morphometry
in male wistar rats supplemented with yacon flour (5-7% fructooligosaccharides)
during 27 days. Yacon flour consumption resulted in a positive Ca and Mg balance,
leading to higher values of bone mineral retention and biomechanical properties
(peak load and stiffness) when compared to the control group. The positive effects
on mineral intestinal absorption, bone mass and biomechanical properties showed an
important role of yacon roots in the maintenance of healthy bones (Lobo et al., 2007Lobo, A. R., Colli, C., Alvares, E. P., & Filisetti, T. M.
(2007). Effects of fructans-containing yacon (Smallanthus sonchifolius Poepp and
Endl.) flour on caecum mucosal morphometry, calcium and magnesium balance, and
bone calcium retention in growing rats. The British Journal of Nutrition, 97(4),
776-785. http://dx.doi.org/10.1017/S0007114507336805.
PMid:17349092
http://dx.doi.org/10.1017/S0007114507336...
).
The prebiotics intake appears to prevent the iron malabsorption and anemia. With the
purpose to evaluate the effect of dietary supplementation with a combination of two
prebiotics (GOS and polydextrose) in iron absorption in gastrectomized rats, Santos et al. (2011)Santos, E. F., Tsuboi, K. H., Araújo, M. R., Falconi, M. A.,
Ouwehand, A. C., Andreollo, N. A., & Miyasaka, C. K. (2011). A ingestão de
prébioticos previne a malabsorção de ferro e anemia induzidas pela
gastrectomia?: Estudo experimental em ratos. ABCD. Arquivos Brasileiros de
Cirurgia Digestiva (São Paulo), 24(1), 9-14.
http://dx.doi.org/10.1590/S0102-67202011000100003.
http://dx.doi.org/10.1590/S0102-67202011...
showed that mice
supplemented had serum iron concentrations significantly higher than those fed the
control diet. Studies in animals have shown that short chain fatty acids, in
particular propionate appears to increase iron absorption in the proximal colon.
This could indicate a potential mechanism by which the intake of prebiotics increase
the availability of dietary iron.
6 Prebiotics, intestinal complications and cancer
The dietary fiber is a wider term that refers to different carbohydrates and lignin that resist hydrolysis by human digestive enzymes, but can be fermented by colonic microflora or partially excreted in the feces. This definition would include within the concept of fiber the no starch polysaccharides (cellulose, hemicellulose, pectins, gums, betaglucans), inulin, FOS, GOS, resistant starch. Some of these fiber components satisfy strictly criteria to be considered as prebiotics (inulin, FOS, GOS, soy oligosaccharides) (World Health Organization, 2004World Health Organization – WHO. (2004). Diet, nutrition and prevention of chronic diseases: report of a joint WHO/FAO expert consultation (WHO Technical Report Series, 916, pp. 1-149). Geneva: WHO.).
In this topic we will highlight some complications and intestinal diseases such as
diarrhea, ulcerative colitis and colon cancer. Prebiotics have been studied less
extensively, however, they may become an ideal treatment or co-treatment option due
to their capacity to increase endogenous lactobacillus and bifidobacteria.
Probiotics and prebiotics may offer a new therapeutic option for the treatment of
inflammatory bowel disease, however, a greater understanding of the mechanisms
behind their action on the gastrointestinal microbiota is required in order to
determine which probiotic, prebiotic or combinations there are the most beneficial
(Geier et al., 2007Geier, M. S., Butler, R. N., & Howarth, G. S. (2007).
Inflammatory bowel disease: current insights into pathogenesis and new
therapeutic options; probiotics, prebiotics and synbiotics. International
Journal of Food Microbiology, 115(1), 1-11.
http://dx.doi.org/10.1016/j.ijfoodmicro.2006.10.006.
PMid:17137666
http://dx.doi.org/10.1016/j.ijfoodmicro....
).
The use of prebiotics as unique treatment or associated with probiotic (symbiotic) also proposed in inflammatory bowel disease in brackets by its effect on the growth of endogenous lactobacilli and bifidobacteria, favoring: the production of short chain fatty acids (especially butyrate , which is a preferential nutrient to enterocytes), prevention of adhesion of pathogenic bacteria, production of antibiotics and decreased intraluminal pH (Olveira Fuster & González-Molero, 2007Olveira Fuster, G., & González-Molero, I. (2007). Probióticos y prebióticos en la práctica clínica. Nutrición Hospitalaria, 22(Suppl 2), 26-34. PMid:17679291.).
Prebiotics improves the function or viability of probiotics via their fermentation,
but their effect on the adherence of probiotics is still unclear. Kadlec & Jakubec (2014)Kadlec, R., & Jakubec, M. (2014). The effect of prebiotics on
adherence of probiotics. Journal of Dairy Science, 97(4), 1983-1990.
http://dx.doi.org/10.3168/jds.2013-7448. PMid:24485681
http://dx.doi.org/10.3168/jds.2013-7448...
, examined the
effect of 4 commercially available prebiotics and 3 simple saccharides (glucose,
galactose, and lactose) on the adherence of 5 probiotic type strains, 2 lactococci
starter cultures, and 5 potential dairy probiotic strains. Adherence was tested in
microtiter plates with porcine mucus or cocultures of the human colon cell lines
Caco2 and HT29. Prebiotics decreased adherence of the tested strains observed on all
types of substrate.
Orrhage et al. (1994)Orrhage, K., Sillerström, E., Gustafsson, J. A., Nord, C. E., &
Rafter, J. (1994). Binding of mutagenic heterocyclic amines by intestinal and
lactic acid bacteria. Mutation Research, 311(2), 239-248.
http://dx.doi.org/10.1016/0027-5107(94)90182-1. PMid:7526189
http://dx.doi.org/10.1016/0027-5107(94)9...
assumed selected
microorganisms would be able to protect the host against carcinogenic activities
through three mechanisms: Probiotics were able to inhibit the bacteria responsible
for converting pre-carcinogenic substances (example polycyclic aromatic hydrocarbons
and nitrosamines) in carcinogenic; Studies on lab animals have shown that some
probiotic directly inhibit the formation of tumor cells; Some bacteria of the gut
flora has demonstrated ability to link and carcinogenic inactivation.
Research has been carried out to study the effect of prebiotics in the response of
acute phase proteins in patients with hematological cancer submitted to
chemotherapy. The supplemented group, corroborating other studies showed significant
increase in the amount of bifidobacteria. The study suggests that bifidobacteria
might have supported the reduction of inflammatory processes and consequently lower
metabolic demand like a protein catabolism (Búrigo
et al., 2007Búrigo, T., Fagundes, R. L. M., Trindade, E. B. S. M., Vasconcelos,
H. C. F. F., Massaut, I. H. B., & Rotolo, M. A. S. (2007). Ação do
prebiótico sobre as proteínas de fase aguda de pacientes com neoplasia
hematológica. Rev Bras Hematol Hemoter, 29(2), 130-135.
http://dx.doi.org/10.1590/S1516-84842007000200010.
http://dx.doi.org/10.1590/S1516-84842007...
).
Although many studies demonstrating the importance of prebiotics and probiotics in health maintenance and prevention of intestinal diseases and cancer, their intake is not common in diets of most of the world population. In this case, health professionals such as health professionals, should be responsible for keeping people informed and encourage the use of functional ingredients containing pro and prebiotics, making it a daily practice in food.
A summary of the main benefits imparted to the consumption of prebiotics is indicated in Figure 1. Many the functions of prebiotics are part of the portfolio of probiotics functions, as the promoter of such benefits relies in the modulated microbiota.
7 Prebiotics and diabetes mellitus: what is the relationship?
There is evidence that the soluble fiber contributes to the reduction of serum
glucose and insulin postprandial by increasing the viscosity of the content of
nutrients in the small intestine, which delays the release of glucose, glucose
connection with the fiber, reducing thus its availability for use, and inhibiting
the action of amylase on amido. Inulin and FOS are good gel-forming agents and as
such influence the absorption of nutrients, in particular carbohydrate, delaying
gastric emptying and/or decreasing the transit time in the intestine delgado (Saad, 2006Saad, S. M. I. (2006). Probióticos e prebióticos: o estado da arte.
Revista Brasileira de Ciências Farmacêuticas, 42(1), 1-16.
http://dx.doi.org/10.1590/S1516-93322006000100002.
http://dx.doi.org/10.1590/S1516-93322006...
).
Besides the use of inulin and its derivatives in office technology, it is important to highlight its health benefits, the first of these is its function as dietary fiber, with the physiological effects attributed to this type of compound, such as decreased levels of lipid and glucose blood and its laxative effect. Another effect is the proven ability of inulin modulate the intestinal flora, this is due to its prebiotic effect. The mechanism by which glucose control occurs through the consumption of yacon is still not clearly. One possible explanation is that the components inulin and FOS are very same of soluble fiber, producing slower glucose absorption, characterizing it as a complementary treatment (Albuquerque & Rolim, 2011Albuquerque, E. N., & Rolim, P. M. (2011). Potencialidades do yacon () no diabetes Mellitus. Smallanthus sonchifoliusRevista de Ciências Médicas, 20(3/4), 99-108.).
Research to examine the effects of prebiotic supplementation on satiety and related
hormones during a test meal for human volunteers by using a noninvasive micromethod
for blood sampling to measure plasma gut peptide concentrations was made by Cani et al. (2009)Cani, P. D., Lecourt, E., Dewulf, E. M., Sohet, F. M., Pachikian, B.
D., Naslain, D., De Backer, F., Neyrinck, A. M., & Delzenne, N. M. (2009).
Gut microbiota fermentation of prebiotics increases satietogenic and incretin
gut peptide production with consequences for appetite sensation and glucose
response after a meal. The American Journal of Clinical Nutrition, 90(5),
1236-1243. http://dx.doi.org/10.3945/ajcn.2009.28095.
PMid:19776140
http://dx.doi.org/10.3945/ajcn.2009.2809...
and they found that
prebiotic supplementation was associated with an increase in plasma gut peptide
concentrations (glucagon-like peptide 1 and peptide YY), which may contribute in
part to changes in appetite sensation and glucose excursion responses after a meal
in healthy subjects.
Another research about arabinoxylans showed main non-starch polysaccharides fraction in many cereal grains. Recent in vitro studies point out that a specific concentrate of long-chain water-extractable arabinoxylans (LC-AX) stimulates specific intestinal microbes like Bifidobacterium longum and launches specific fermentation patterns with potential health benefits for the host (e.g. propionate production). Human trials demonstrate that a long-term administration of LC-AX can restore the glucose and insulin responses in patients suffering from diabetes type II (Van den Abbeele et al., 2011Van den Abbeele P., Van den Wiele, T., & Possemiers, S. (2011). Prebiotic effect and potential health benefit of arabinoxylans. Agro Food Industry Hi-Tech, 22(Suppl. 2), 9-12.).
Functional foods have become the prized of food innovation in the past few years. All big food companies are investing in functional foods because the mega trends in society seem to require healthy food with added benefits to improve the health, wellness and people life quality.
8 Development of products with prebiotic allegation
Nowadays one of the tendencies in food segment is the healthiness and wellness, associated to the growth of food industry in answering the consumer exigencies who is more conscious that an adequate feeding with healthy ingredients are indispensable to a better life wellness to children and adults.
Many researches about of developing food products, involving milk and derivatives, bread, cake, etc., adding value due contain prebiotic ingredients and organisms. It is valid to highlight that these products must positively answer to the nutritional and sensory characteristics, and remain in appropriate conditions during the processing and storage. Studies show that the counting of probiotic bacteria in products already commercialized, especially the milk derivate, are found inside the minimal boundaries recommended, keeping this way a good condition in viability during their shelf lives (Barreto et al., 2003Barreto, G. P. M., Silva, N., Silva, E. N., Botelho, L., Yim, D. K., Almeida, C. G., & Saba, G. L. (2003). Quantificação de Lactobacillus acidophilus, bifidobactérias e bactérias totais em produtos probióticos comercializados no Brasil. Brazilian Journal of Food Technology, 6(1), 119-126.). Food applications are illustrated in Table 1.
Prebiotics has also being used in child formulation (Millani et al., 2009Millani, E., Konstantyner, T., & Taddei, J. A. A. C. (2009).
Effects of prebiotics (oligosaccharides) use on child’s health. Revista Paulista
de Pediatria, 27(4), 436-446.
http://dx.doi.org/10.1590/S0103-05822009000400014.
http://dx.doi.org/10.1590/S0103-05822009...
) in a way to answer children questions about no
have access mother’s milk or partially received it. Consumption of these products
evidence improvements in allergy cases, crying and colic increase, improvement in
the prevention of constipation, among others. However, food industry must be
cautious into incorporate prebiotics to child food, considering that studies are
still necessary in this area.
A very used ingredient, nowadays, in the development of new products is the yacon potato (Smallanthus sonchifolius), tubercle from the Andes that has been featured because it is rich in FOS and inulin. Yacon can suffer different types of processing to obtain pulps, juices and flours, and these are being added to other food.
As adding yacon potato to breads, Rolim et al.
(2011)Rolim, P. M., Salgado, S. M., Padilha, V. M., Livera, A. V. S.,
Andrade, S. A. C., & Guerra, N. B. (2011). Glycemic profile and prebiotic
potential "in vitro" of bread with yacon (Smallanthus sonchifolius) flour. Food
Science and Technology (Campinas), 31(2), 467-474.
http://dx.doi.org/10.1590/S0101-20612011000200029.
http://dx.doi.org/10.1590/S0101-20612011...
verified a rich in fiber food, low glycemic index and considerable
prebiotic effect, in presenting the bifidobacteria counting and lactobacilli between
107 a 1010 (UFCmL–1), possibly being able of
colonizing the intestines, once that the minimal recommendation to make the
probiotics effects is 106 UFCmL–1. Researchers also evaluated
the effects of yacon potato flour addition in chocolate cakes, as an alternative in
substituting sugar, and had positive results in terms of chemical composition,
glycemic index and charge and satisfactory prebiotic capacity (Padilha et al., 2010Padilha, V. M., Rolim, P. M., Salgado, S. M., Livera, A. S.,
Andrade, S. A. C., & Guerra, N. B. (2010). Perfil sensorial de bolos de
chocolate formulados com farinha de yacon (Smallanthus sonchifolius). Food
Science and Technology (Campinas), 30(3), 735-740.
http://dx.doi.org/10.1590/S0101-20612010000300026.
http://dx.doi.org/10.1590/S0101-20612010...
).
To evaluate the prebiotic effect of a new product, models may be used. Samples can be
submitted to the process of fermentation with anaerobic system and addition of an
inoculum prepared from the infants faeces.The liquid is used for metabolic bacterial
count homo and hetero-fermentative, as well as providing analysis of short-chain
fatty acids (SCFA). To count the bacteria can use the differential medium agar also
generating system anaerobic. And analysis of SCFA can be performed by gas
chromatography (Barry et al.,1995Barry, J. L., Hoebler, C., Macfarlane, G. T., Macfarlane, S.,
Mathers, J. C., Reed, K. A., Mortensen, P. B., Nordgaard, I., Rowland, I. R.,
& Rumney, C. J. (1995). Estimation of the fermentability of dietary fibre in
vitro: a European interlaboratory study. The British Journal of Nutrition,
74(3), 303-322. http://dx.doi.org/10.1079/BJN19950137.
PMid:7547846
http://dx.doi.org/10.1079/BJN19950137...
; Vanderzant & Splittsloesser, 2001Vanderzant, C., & Splittsloesser, D. F. (2001). Compendium of
methods for the microbiological examination of foods (4th ed.). Washington:
American Public Health Association.).
Rodrigues et al. (2012)Rodrigues, D., Rocha-Santos, T. A. P., Gomes, A. M., Goodfellow, B.
J., & Freitas, A. C. (2012). Lipolysis in probiotic and symbiotic cheese:
the influence of probiotic bacteria, prebiotic compounds and ripening time on
free fatty acid profiles. Food Chemistry, 131(4), 1414-1421.
http://dx.doi.org/10.1016/j.foodchem.2011.10.010.
http://dx.doi.org/10.1016/j.foodchem.201...
, investigated the
influence of FOS and inulin (50:50) on the free fatty acid profile of cheese, with
special emphasis on the conjugated linoleic acid. Linoleic acid content increase
during the ripening time suggests the addition of prebiotics in probiotic cheese, to
improve quality with lower atherogenicity index.
It is also possible to measure the effect of a prebiotic potential by evaluating the
resistance of microorganisms to acid, can be done replied with Man Rogosa Sharp
(MRS) broth with accompanying the pH. Other method to evaluate microorganisms it is
the resistance to bile using lyophilized bovine bile for monitoring the cell
viability at different times (Rönkä et al.,
2003Rönkä, E., Malinen, E., Saarela, M., Rinta-Koski, M., Aarnikunnas,
J., & Palva, A. (2003). Probiotic and milk technological properties of
Lactobacillus brevis. International Journal of Food Microbiology, 83(1), 63-74.
http://dx.doi.org/10.1016/S0168-1605(02)00315-X. PMid:12672593
http://dx.doi.org/10.1016/S0168-1605(02)...
; De Man et al., 1960De Man, J. C., Rogosa, M., & Sharpe, M. E. (1960). A medium for
the cultivation of Lactobacilli. The Journal of Applied Bacteriology, 23(1),
130-135. http://dx.doi.org/10.1111/j.1365-2672.1960.tb00188.x.
http://dx.doi.org/10.1111/j.1365-2672.19...
).
Promising research with prebiotics can be produced by sugar solution through
transfructosylated reaction (Aachary &
Prapulla, 2009Aachary, A. A., & Prapulla, S. G. (2009). Value addition to
spent osmotic sugar solution (SOS) by enzymatic conversion to
fructooligosaccharides (FOS), a low calorie prebiotic. Innovative Food Science
& Emerging Technologies, 10(2), 284-288.
http://dx.doi.org/10.1016/j.ifset.2008.11.013.
http://dx.doi.org/10.1016/j.ifset.2008.1...
). The solid wastes accumulated in industries when sucrose
saturated solutions can synthesize fructooligosaccharides. (Gullón et al., 2011Gullón, P., González-Muñoz, M. J., & Parajó, J. C. (2011).
Manufacture and prebiotic potential of oligosaccharides derived from industrial
solid wastes. Bioresource Technology, 102(10), 6112-6119.
http://dx.doi.org/10.1016/j.biortech.2011.02.059. PMid:21392971
http://dx.doi.org/10.1016/j.biortech.201...
).
Recent technic like a Ultrasound assisted extraction (UAE) also was used to extract
oligosaccharides from selected fruits (blueberry, nectarine, raspberry, watermelon)
and vegetables (garlic, Jerusalem artichoke, leek, scallion, spring garlic and white
onion). UAE increased the concentration of extracted oligosaccharides in all fruits
and vegetables from 2 to 4-fold compared to conventional extraction (Jovanovic-Malinovska et al., 2015Jovanovic-Malinovska, R., Kuzmanova, S., & Winkelhausen, E.
(2015). Application of ultrasound for enhanced extraction of prebiotic
oligosaccharides from selected fruits and vegetables. Ultrasonics Sonochemistry,
22, 446-453. http://dx.doi.org/10.1016/j.ultsonch.2014.07.016.
PMid:25116595
http://dx.doi.org/10.1016/j.ultsonch.201...
).
9 Effect of prebiotic in sensory acceptance of foods
Sensory analysis is a decisive phase during the food product development. Morais et al. (2014)Morais, E. C., Morais, A. R., Cruz, A. G., & Bolini, H. M. A.
(2014). Development of chocolate dairy dessert with addition of prebiotics and
replacement of sucrose with different high-intensity sweeteners. Journal of
Dairy Science, 97(5), 2600-2609. http://dx.doi.org/10.3168/jds.2013-7603.
PMid:24612793
http://dx.doi.org/10.3168/jds.2013-7603...
developed chocolate dairy
dessert with addition of prebiotics and replacement of sucrose with different
high-intensity sweeteners. The relative sweetness analysis showed that sweeteners
had the highest sweetening power compared with the prebiotic chocolate dairy dessert
containing 8% sucrose. The study of sweetness in this product is important because
consumers desire healthier functional products with no added sugar.
Cruz et al. (2013)Cruz, A. G., Cavalcanti, R. N., Guerreiro, L. M. R., Sant’Ana, A.
S., Nogueira, L. C., Oliveira, C. A. F., Deliza, R., Cunha, R. L., Faria, J. A.
F., & Bolini, H. M. A. (2013). Developing a prebiotic yogurt: rheological,
physico-chemical and microbiological aspects and adequacy of survival analyses
methodology. Journal of Food Engineering, 114(3), 323-330.
http://dx.doi.org/10.1016/j.jfoodeng.2012.08.018.
http://dx.doi.org/10.1016/j.jfoodeng.201...
aimed to evaluate the
effect of increasing concentrations of oligofructose addition on physicochemical,
rheological and microbiological characteristics of non-flavored yogurt. The addition
of oligofructose showed no influence on the pH, proteolysis or the viability of
Streptococcus thermophilus or Lactobacillus
bulgaricus during 28 days of refrigerated storage
(p > 0.05).
In another study, inulin was supplemented in bread and results are smaller loaves,
harder crumb and darker colour. Sensory studies reflected acceptability decreases
with inulin content, yeast invertase and dry heat degrade inulin, and
fructo-oligosaccharide/inulin fortification in bread at 5% seems achievable (Morris & Morris, 2012Morris, C., & Morris, G. A. (2012). The effect of inulin and
fructo-oligosaccahride supplementation on the textural, rheological and sensory
properties of bread and their role in wheigh management: a review. Food
Chemistry, 133(2), 237-248.
http://dx.doi.org/10.1016/j.foodchem.2012.01.027.
http://dx.doi.org/10.1016/j.foodchem.201...
).
Study to determine the effect of a prebiotic (fructooligosaccharide) on the sensory
properties and consumer acceptability of peach-flavored drinkable yogurts was carry
out. The yogurts containing the prebiotic were not significantly different from
their comparable controls indicating that a prebiotic can be added without impacting
acceptance (Gonzalez et al., 2011[REMOVED IF= FIELD]Gonzalez, N. J., Adhikari, K., Sancho-Madriz,
& M. F. (2011). Sensory characteristics of peach-flavoured yoghurt drinks
containing prebiotics and synbiotics. LWT - Food Science Technology, 44(1),
158-163. http://dx.doi.org/10.1016/j.lwt.2010.06.008.
http://dx.doi.org/10.1016/j.lwt.2010.06....
).
10 Functional food market: a real tendency
Functional and food ingredients offer benefits to human health: gastrointestinal, cardiovascular, system growth, development, cell differentiation, behavior of functions physiological and as antioxidants. Foods which naturally contains bioactive compounds. Euromonitor International data about food and drink markets associated with health and wellbeing, achieved US$750 billion in 2013. In this context, US$ 264 billion represents only the functional or fortified products, foods and drinks have special ingredients to bring in formulas to health benefits for consumers. Currently, Latin America, has US$ 45 billion or 17% of the functional food and drinks market.
Aligned with the trends of this market, many industries have invested in scientific research and technological innovation in the development of products referenced by their functional properties. This segment includes different types of functional ingredients for the industry food, being used in bakery foods, cereals, drinks and dairy products, and the segment of food supplements. Taking advantage moment, brazilian producers are increasingly investing in these foods that have become trend. In contrast, some challenges are detected, such as the limitations imposed by regulator organ in relation to claims of product benefits, the delay in the registration period, the lack of clinical trials to advance the applicability of the products and the difficulty of researching new substances originated mainly from native flora. Even so, the category of functional foods featured 91 new records in 2013, against 178 recorded between 2011 and 2012. Currently, the total number of approved products reaches 734, mainly in the segments allegations functional health and bioactive substances and probiotics with claims of health or functional properties.
11 Conclusions
During this chapter it was tried to prove the relevance of prebiotics in the benefits of probiotics and its appliances in food products. However, new analytics analyses are necessary with instrumental methods to determine the fructan fractions in raw material and products, as well as characterize in a selective way the probiotic bacteria using specific collective ways to these genres. Introduction of functional compounds like prebiotics in the diet seems to be an attractive alternative. Owing to its wide range of preventive and therapeutic possibilities prebiotics research certainly catching momentum.
-
Practical Application: Innovative applicability to the prebiotics is a consumer attitude for maximum efficacy of their functionality.
References
- Aachary, A. A., & Prapulla, S. G. (2009). Value addition to spent osmotic sugar solution (SOS) by enzymatic conversion to fructooligosaccharides (FOS), a low calorie prebiotic. Innovative Food Science & Emerging Technologies, 10(2), 284-288. http://dx.doi.org/10.1016/j.ifset.2008.11.013.
» http://dx.doi.org/10.1016/j.ifset.2008.11.013 - Albuquerque, E. N., & Rolim, P. M. (2011). Potencialidades do yacon () no diabetes Mellitus. Smallanthus sonchifoliusRevista de Ciências Médicas, 20(3/4), 99-108.
- Barreto, G. P. M., Silva, N., Silva, E. N., Botelho, L., Yim, D. K., Almeida, C. G., & Saba, G. L. (2003). Quantificação de Lactobacillus acidophilus, bifidobactérias e bactérias totais em produtos probióticos comercializados no Brasil. Brazilian Journal of Food Technology, 6(1), 119-126.
- Barry, J. L., Hoebler, C., Macfarlane, G. T., Macfarlane, S., Mathers, J. C., Reed, K. A., Mortensen, P. B., Nordgaard, I., Rowland, I. R., & Rumney, C. J. (1995). Estimation of the fermentability of dietary fibre in vitro: a European interlaboratory study. The British Journal of Nutrition, 74(3), 303-322. http://dx.doi.org/10.1079/BJN19950137. PMid:7547846
» http://dx.doi.org/10.1079/BJN19950137 - Berg, R. D. (1996). The indigenous gastrointestinal microflora. Trends in Microbiology, 4(11), 430-435. http://dx.doi.org/10.1016/0966-842X(96)10057-3. PMid:8950812
» http://dx.doi.org/10.1016/0966-842X(96)10057-3 - Bruzzese, E., Volpicelli, M., Squeglia, V., Bruzzese, D., Salvini, F., Bisceglia, M., Lionetti, P., Cinquetti, M., Iacono, G., Amarri, S., & Guarino, A. (2009). A formula containing galacto- and fructo-oligosaccharides prevents intestinal and extra-intestinal infections: an observational study. Clinical Nutrition (Edinburgh, Scotland), 28(2), 156-161. http://dx.doi.org/10.1016/j.clnu.2009.01.008. PMid:19231042
» http://dx.doi.org/10.1016/j.clnu.2009.01.008 - Burgain, J., Gaiani, C., Linder, M., & Scher, J. (2011). Encapsulation of probiotic living cells: From laboratory scale to industrial applications. Journal of Food Engineering, 104(4), 467-483. http://dx.doi.org/10.1016/j.jfoodeng.2010.12.031.
» http://dx.doi.org/10.1016/j.jfoodeng.2010.12.031 - Búrigo, T., Fagundes, R. L. M., Trindade, E. B. S. M., Vasconcelos, H. C. F. F., Massaut, I. H. B., & Rotolo, M. A. S. (2007). Ação do prebiótico sobre as proteínas de fase aguda de pacientes com neoplasia hematológica. Rev Bras Hematol Hemoter, 29(2), 130-135. http://dx.doi.org/10.1590/S1516-84842007000200010.
» http://dx.doi.org/10.1590/S1516-84842007000200010 - Buriti, F. C. A., & Saad, S. M. I. (2007). Bactérias do grupo Lactobacillus casei: caracterização, viabilidade como probióticos em alimentos e sua importância para a saúde humana. Archivos Latinoamericanos de Nutrición, 57(4), 373-380. PMid:18524322.
- Cani, P. D., Lecourt, E., Dewulf, E. M., Sohet, F. M., Pachikian, B. D., Naslain, D., De Backer, F., Neyrinck, A. M., & Delzenne, N. M. (2009). Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. The American Journal of Clinical Nutrition, 90(5), 1236-1243. http://dx.doi.org/10.3945/ajcn.2009.28095. PMid:19776140
» http://dx.doi.org/10.3945/ajcn.2009.28095 - Cherbut, C. (2002). Inulin and oligofructose in the dietary fibre concept. The British Journal of Nutrition, 87(Suppl. 2), S159-S162. http://dx.doi.org/10.1079/BJN2002532. PMid:12088513
» http://dx.doi.org/10.1079/BJN2002532 - Coman, M. M., Cecchini, C., Verdenelli, M. C., Silvi, S., Orpianesi, C., & Cresci, A. (2012). Functional foods as carriers for SYNBIO®, a probiotic bacteria combination. International Journal of Food Microbiology, 157(3), 346-352. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.06.003. PMid:22727086
» http://dx.doi.org/10.1016/j.ijfoodmicro.2012.06.003 - Cruz, A. G., Cavalcanti, R. N., Guerreiro, L. M. R., Sant’Ana, A. S., Nogueira, L. C., Oliveira, C. A. F., Deliza, R., Cunha, R. L., Faria, J. A. F., & Bolini, H. M. A. (2013). Developing a prebiotic yogurt: rheological, physico-chemical and microbiological aspects and adequacy of survival analyses methodology. Journal of Food Engineering, 114(3), 323-330. http://dx.doi.org/10.1016/j.jfoodeng.2012.08.018.
» http://dx.doi.org/10.1016/j.jfoodeng.2012.08.018 - Cummings, J. H., & Macfarlane, G. T. (2002). Gastrointestinal effects of prebiotics. The British Journal of Nutrition, 87(Suppl. 2), S145-S151. http://dx.doi.org/10.1079/BJN/2002530. PMid:12088511
» http://dx.doi.org/10.1079/BJN/2002530 - De Man, J. C., Rogosa, M., & Sharpe, M. E. (1960). A medium for the cultivation of Lactobacilli. The Journal of Applied Bacteriology, 23(1), 130-135. http://dx.doi.org/10.1111/j.1365-2672.1960.tb00188.x.
» http://dx.doi.org/10.1111/j.1365-2672.1960.tb00188.x - Delgado, G. T. C., Tamashiro, W. M. S. C., Maróstica Junior, M. R., Moreno, Y. M. F., & Pastore, G. M. (2011). The putative effects of prebiotics as immunomodulatory agents. Food Research International, 44(10), 3167-3173. http://dx.doi.org/10.1016/j.foodres.2011.07.032.
» http://dx.doi.org/10.1016/j.foodres.2011.07.032 - Geier, M. S., Butler, R. N., & Howarth, G. S. (2007). Inflammatory bowel disease: current insights into pathogenesis and new therapeutic options; probiotics, prebiotics and synbiotics. International Journal of Food Microbiology, 115(1), 1-11. http://dx.doi.org/10.1016/j.ijfoodmicro.2006.10.006. PMid:17137666
» http://dx.doi.org/10.1016/j.ijfoodmicro.2006.10.006 - Gibson, G. R., & Fuller, R. (2000). Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. The Journal of Nutrition, 130(Suppl. 2), 391S-395S. PMid:10721913.
- Gibson, G. R., & Roberfroid, M. B. (1995). Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. The Journal of Nutrition, 125(6), 1401-1412. PMid:7782892.
- [REMOVED IF= FIELD]Gonzalez, N. J., Adhikari, K., Sancho-Madriz, & M. F. (2011). Sensory characteristics of peach-flavoured yoghurt drinks containing prebiotics and synbiotics. LWT - Food Science Technology, 44(1), 158-163. http://dx.doi.org/10.1016/j.lwt.2010.06.008.
» http://dx.doi.org/10.1016/j.lwt.2010.06.008 - Gullón, P., González-Muñoz, M. J., & Parajó, J. C. (2011). Manufacture and prebiotic potential of oligosaccharides derived from industrial solid wastes. Bioresource Technology, 102(10), 6112-6119. http://dx.doi.org/10.1016/j.biortech.2011.02.059. PMid:21392971
» http://dx.doi.org/10.1016/j.biortech.2011.02.059 - Jovanovic-Malinovska, R., Kuzmanova, S., & Winkelhausen, E. (2015). Application of ultrasound for enhanced extraction of prebiotic oligosaccharides from selected fruits and vegetables. Ultrasonics Sonochemistry, 22, 446-453. http://dx.doi.org/10.1016/j.ultsonch.2014.07.016. PMid:25116595
» http://dx.doi.org/10.1016/j.ultsonch.2014.07.016 - Kadlec, R., & Jakubec, M. (2014). The effect of prebiotics on adherence of probiotics. Journal of Dairy Science, 97(4), 1983-1990. http://dx.doi.org/10.3168/jds.2013-7448. PMid:24485681
» http://dx.doi.org/10.3168/jds.2013-7448 - Lajolo, F. M., & Menezes, E. W. (2006). Carbohidratos en alimentos regionales Iberoamericanos. São Paulo: Universidade de São Paulo.
- Lobo, A. R., Colli, C., Alvares, E. P., & Filisetti, T. M. (2007). Effects of fructans-containing yacon (Smallanthus sonchifolius Poepp and Endl.) flour on caecum mucosal morphometry, calcium and magnesium balance, and bone calcium retention in growing rats. The British Journal of Nutrition, 97(4), 776-785. http://dx.doi.org/10.1017/S0007114507336805. PMid:17349092
» http://dx.doi.org/10.1017/S0007114507336805 - Mann, J., Cummings, J. H., Englyst, H. N., Key, T., Liu, S., Riccardi, G., Summerbell, C., Uauy, R., van Dam, R. M., Venn, B., Vorster, H. H., & Wiseman, M. (2007). FAO/WHO scientific update on carbohydrates in human nutrition: conclusions. European Journal of Clinical Nutrition, 61(Suppl. 1), S132-S137. http://dx.doi.org/10.1038/sj.ejcn.1602943. PMid:17992184
» http://dx.doi.org/10.1038/sj.ejcn.1602943 - Menne, E., Guggenbuhl, N., & Roberfroid, M. (2000). Fn-type chicory inulin hydrolysate has a prebiotic effect in humans. The Journal of Nutrition, 130(5), 1197-1199. PMid:10801918.
- Millani, E., Konstantyner, T., & Taddei, J. A. A. C. (2009). Effects of prebiotics (oligosaccharides) use on child’s health. Revista Paulista de Pediatria, 27(4), 436-446. http://dx.doi.org/10.1590/S0103-05822009000400014.
» http://dx.doi.org/10.1590/S0103-05822009000400014 - Morais, E. C., Morais, A. R., Cruz, A. G., & Bolini, H. M. A. (2014). Development of chocolate dairy dessert with addition of prebiotics and replacement of sucrose with different high-intensity sweeteners. Journal of Dairy Science, 97(5), 2600-2609. http://dx.doi.org/10.3168/jds.2013-7603. PMid:24612793
» http://dx.doi.org/10.3168/jds.2013-7603 - Morris, C., & Morris, G. A. (2012). The effect of inulin and fructo-oligosaccahride supplementation on the textural, rheological and sensory properties of bread and their role in wheigh management: a review. Food Chemistry, 133(2), 237-248. http://dx.doi.org/10.1016/j.foodchem.2012.01.027.
» http://dx.doi.org/10.1016/j.foodchem.2012.01.027 - Olveira Fuster, G., & González-Molero, I. (2007). Probióticos y prebióticos en la práctica clínica. Nutrición Hospitalaria, 22(Suppl 2), 26-34. PMid:17679291.
- Orrhage, K., Sillerström, E., Gustafsson, J. A., Nord, C. E., & Rafter, J. (1994). Binding of mutagenic heterocyclic amines by intestinal and lactic acid bacteria. Mutation Research, 311(2), 239-248. http://dx.doi.org/10.1016/0027-5107(94)90182-1. PMid:7526189
» http://dx.doi.org/10.1016/0027-5107(94)90182-1 - Padilha, V. M., Rolim, P. M., Salgado, S. M., Livera, A. S., Andrade, S. A. C., & Guerra, N. B. (2010). Perfil sensorial de bolos de chocolate formulados com farinha de yacon (Smallanthus sonchifolius). Food Science and Technology (Campinas), 30(3), 735-740. http://dx.doi.org/10.1590/S0101-20612010000300026.
» http://dx.doi.org/10.1590/S0101-20612010000300026 - Passariello, A., Terrin, G., De Marco, G., Cecere, G., Ruotolo, S., Marino, A., Cosenza, L., Tardi, M., Nocerino, R., & Berni Canani, R. (2011). Efficacy of a new hypotonic oral rehydration solution containing zinc and prebiotics in the treatment of childhood acute diarrhea: a randomized controlled trial. The Journal of Pediatrics, 158(2), 288-92.e1. http://dx.doi.org/10.1016/j.jpeds.2010.07.055. PMid:20828714
» http://dx.doi.org/10.1016/j.jpeds.2010.07.055 - Peña, A. S. (2007). Flora intestinal, probióticos, prebióticos, simbióticos y alimentos novedosos. Revista Espanola de Enfermedades Digestivas, 99(11), 653-658. http://dx.doi.org/10.4321/S1130-01082007001100006. PMid:18271664
» http://dx.doi.org/10.4321/S1130-01082007001100006 - Perrin, S., Fougnies, C., Grill, J. P., Jacobs, H., & Schneider, F. (2002). Fermentation of chicory fructo-oligosaccharides in mixtures of different degrees of polymerization by three strains of bifidobacteria. Canadian Journal of Microbiology, 48(8), 759-763. http://dx.doi.org/10.1139/w02-065. PMid:12381033
» http://dx.doi.org/10.1139/w02-065 - Priebe, M. G., Vonk, R. J., Sun, X., He, T., Harmsen, H. J., & Welling, G. W. (2002). The physiology of colonic metabolism. Possibilities for interventions with pre- and probiotics. European Journal of Nutrition, 41(Suppl. 1), I2-I10. PMid:12420110.
- Quinteros, E. T. T. (2000). Produção com tratamento enzimático e avaliação do suco de yacon (Tese de Doutorado). Faculdade de Engenharia de Alimentos, Universidade Estadual de Campinas, Campinas.
- Rafter, J., Bennett, M., Caderni, G., Clune, Y., Hughes, R., Karlsson, P. C., Klinder, A., O’Riordan, M., O’Sullivan, G. C., Pool-Zobel, B., Rechkemmer, G., Roller, M., Rowland, I., Salvadori, M., Thijs, H., Van Loo, J., Watzl, B., & Collins, J. K. (2007). Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. The American Journal of Clinical Nutrition, 85(2), 488-496. PMid:17284748.
- Roberfroid, M. B. (2005). Introducing inulin-type fructans. The British Journal of Nutrition, 93(Suppl. 1), S13-S25. http://dx.doi.org/10.1079/BJN20041350. PMid:15877886
» http://dx.doi.org/10.1079/BJN20041350 - Rodrigues, D., Rocha-Santos, T. A. P., Gomes, A. M., Goodfellow, B. J., & Freitas, A. C. (2012). Lipolysis in probiotic and symbiotic cheese: the influence of probiotic bacteria, prebiotic compounds and ripening time on free fatty acid profiles. Food Chemistry, 131(4), 1414-1421. http://dx.doi.org/10.1016/j.foodchem.2011.10.010.
» http://dx.doi.org/10.1016/j.foodchem.2011.10.010 - Rolim, P. M., Salgado, S. M., Padilha, V. M., Livera, A. V. S., Andrade, S. A. C., & Guerra, N. B. (2011). Glycemic profile and prebiotic potential "in vitro" of bread with yacon (Smallanthus sonchifolius) flour. Food Science and Technology (Campinas), 31(2), 467-474. http://dx.doi.org/10.1590/S0101-20612011000200029.
» http://dx.doi.org/10.1590/S0101-20612011000200029 - Romeo, J., Nova, E., Wärnberg, J., Gómez-Martínez, S., Díaz Ligia, L. E., & Marcos, A. (2010). Immunomodulatory effect of fibres, probiotics and synbiotics in different life-stages. Nutrición Hospitalaria, 25(3), 341-349. PMid:20593114.
- Rönkä, E., Malinen, E., Saarela, M., Rinta-Koski, M., Aarnikunnas, J., & Palva, A. (2003). Probiotic and milk technological properties of Lactobacillus brevis. International Journal of Food Microbiology, 83(1), 63-74. http://dx.doi.org/10.1016/S0168-1605(02)00315-X. PMid:12672593
» http://dx.doi.org/10.1016/S0168-1605(02)00315-X - Saad, S. M. I. (2006). Probióticos e prebióticos: o estado da arte. Revista Brasileira de Ciências Farmacêuticas, 42(1), 1-16. http://dx.doi.org/10.1590/S1516-93322006000100002.
» http://dx.doi.org/10.1590/S1516-93322006000100002 - Santos, E. F., Tsuboi, K. H., Araújo, M. R., Falconi, M. A., Ouwehand, A. C., Andreollo, N. A., & Miyasaka, C. K. (2011). A ingestão de prébioticos previne a malabsorção de ferro e anemia induzidas pela gastrectomia?: Estudo experimental em ratos. ABCD. Arquivos Brasileiros de Cirurgia Digestiva (São Paulo), 24(1), 9-14. http://dx.doi.org/10.1590/S0102-67202011000100003.
» http://dx.doi.org/10.1590/S0102-67202011000100003 - Scholtens, P. A., Alles, M. S., Bindels, J. G., van der Linde, E. G., Tolboom, J. J., & Knol, J. (2006). Bifidogenic effects of solid weaning foods with added prebiotic oligosaccharides: a randomised controlled clinical trial. Journal of Pediatric Gastroenterology and Nutrition, 42(5), 553-559. http://dx.doi.org/10.1097/01.mpg.0000221887.28877.c7. PMid:16707980
» http://dx.doi.org/10.1097/01.mpg.0000221887.28877.c7 - Silveira Rodríguez, M. B., Monereo Megías, S., & Molina Baena, B. (2003). Alimentos funcionales y nutrición óptima. Cerca o lejos? Revista Espanola de Salud Publica, 77(3), 317-331. http://dx.doi.org/10.1590/S1135-57272003000300003. PMid:12852326
» http://dx.doi.org/10.1590/S1135-57272003000300003 - Thomas, D. W., Greer, F. R., American Academy of Pediatrics Committee on Nutrition, & American Academy of Pediatrics Section on Gastroenterology, Hepatology, and Nutrition (2010). Probiotics and prebiotics in pediatrics. Pediatrics, 126(6), 1217-1231. http://dx.doi.org/10.1542/peds.2010-2548. PMid:21115585
» http://dx.doi.org/10.1542/peds.2010-2548 - Van den Abbeele P., Van den Wiele, T., & Possemiers, S. (2011). Prebiotic effect and potential health benefit of arabinoxylans. Agro Food Industry Hi-Tech, 22(Suppl. 2), 9-12.
- Vanderzant, C., & Splittsloesser, D. F. (2001). Compendium of methods for the microbiological examination of foods (4th ed.). Washington: American Public Health Association.
- Vulevic, J., Drakoularakou, A., Yaqoob, P., Tzortzis, G., & Gibson, G. R. (2008). Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. The American Journal of Clinical Nutrition, 88(5), 1438-1446. PMid:18996881.
- Wang, Y. (2009). Prebiotics: Present and future in food science and technology. Food Research International, 42(1), 8-12. http://dx.doi.org/10.1016/j.foodres.2008.09.001.
» http://dx.doi.org/10.1016/j.foodres.2008.09.001 - World Health Organization – WHO. (2004). Diet, nutrition and prevention of chronic diseases: report of a joint WHO/FAO expert consultation (WHO Technical Report Series, 916, pp. 1-149). Geneva: WHO.
Publication Dates
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Publication in this collection
Jan-Mar 2015
History
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Received
27 Oct 2014 -
Accepted
26 Jan 2015