Mushroom Probiotics Imp PDF
Mushroom Probiotics Imp PDF
Mushroom Probiotics Imp PDF
Review
There are at least 12, 000 species of fungi that can be considered as mushrooms, with at least 2000 species are edible (Chang, 1999). According to Sanchez (2004) over 200 species have been collected from the wild and used for various traditional medical purposes, mostly in Far East. About 35 species have been cultivated commercially and 20 are cultivated on an industrial scale. The most cultivated mushroom worldwide is A. bisporus (button mushroom), followed by Lentinus edodes (shiitake), Pleurotus spp (oyster mushrooms), Auricula auricula (wood ear mushroom), Flamulina velutipes (winter mushroom) and Volvariella volvacea (straw mushroom). Table 1 summarizes worldwide production of mushroom as updated by the Food and Agriculture Organization of the United Nations (2009). China was found to be the biggest producers for mushrooms, as they produced more than 1.5 million metric tons in the year 2007. This showed an increment of about 65% in 10 years times. This was followed by United States and Canada. Israel and India showed drastic increased in the number of metric tons produced in 10 years, while Singapore and Kazakhstan can be regarded as new beginners as they are producing the least mushrooms since 1997. Production of mushrooms seems to continuously increase over time. This might due to high consumer demand and increase in consumer awareness on the health benets of mushrooms. Thus, this review will emphasize on the scientically proven health benets of mushrooms, recent trend on functional foods and the potential of mushroom as a prebiotic as well as the concept of prebiotic. Health benets of mushrooms Mushrooms have been used not only as a source of food but medicinal resource as well (Wasser, 2002). The medicinal properties of mushrooms have been conrmed through an intensive research conducted worldwide. According to Chang (2001), medicinal mushrooms have been used as a dietary supplement or medicinal food in China for over 2000 years. The extractable ingredients of mushrooms were incorporated in products and were claimed to improve biological function of human body. It had received great attention since the late 1980s. According to Mahajna, Dotan, Zaidman, Petroza, and Wasser (2009), fungi from the Basidiomycota received great interest because it contains large number of biologically active compounds such as polysaccharides,
Introduction Mushroom growing has a long tradition in Eastern Asian countries, especially in China, where it started around 600 A.D. with Auricularia auricular or also known as Wood Ear. In Europe, cultivation of Agaricus bisporus, the button mushroom, was rst achieved in France during the seventeenth century (Kues & Liu, 2000).
* Corresponding author.
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Table 1. Worldwide production of mushroom. Country China United States Canada India Indonesia Republic of Korea Islamic Republic of Iran Vietnam Thailand Israel Jordan Kazakhstan Singapore Production (tonnes) 1997 562,194* 366,810 68,020 9000* 19,000* 13,181 10,000* 10,000* 9000* 1260 500 e e 2007 1,605,000 390,000 81,500 48,000 30,000 28,500 28,000 18,000 10,000 9500 700 500 10 65.0* 5.9* 16.5* 81.3* 36.7* 53.8* 64.3 44.4* 10* 86.7* 28.6* 100* 100* Percentage (%)
glycoproteins, triterpenes and antibiotics (Wasser, 2002). However, among all bioactive compounds, polysaccharide has been extensively studied. Several glycans have been isolated from the fruit bodies, spores and the mycelium of Reishi or Mannentake (Ganoderma lucidum) (Bao, Duan, Fang, & Fang, 2001; Bao, Liu, Fang, & Li, 2001; Liu, Yuan, Chung, & Chen, 2002). Previous studies suggested that these polysaccharides had immunomodulating properties, including the enhancement of lymphocyte proliferation and antibody production (Bao, Liu, et al., 2001) as well as producing both anti-genotoxic and antitumor promoting activities (Kim, Kacew, & Lee, 1999; Sone, Okuda, Wada, Kishida, & Misaki, 1985; Wasser, 2002). Antitumor activity of mushroom polysaccharides (sclerotia of Pleurotus tuber-regium) against human hepatic cancer cell has been observed by Tao, Zhang, and Cheung (2006). Other than that, polysaccharides isolated from the fruiting bodies of Pleurotus ostreatus have also been proven to exert antitumor activity against Hela tumor cell (Tong et al., 2009). The sporoderm-broken germinating spores (SBGS) of Reishi were also found to show a signicant antitumor effect, especially in the prevention of the recrudescence or metastasis of cancerous cells. It mitigates the toxic and side effects of radiotherapy and chemotherapy in some patients (Bao, Liu, et al., 2001). These polysaccharides are of different chemical composition, with most belonging to the group of b-glucans. In order to exhibit their antitumor activity, the main chain of the glucan have to be b-(1 / 3) linkages with additional b(1 / 6) branch points (Wasser, 2002). The antitumor activities of Reishi polysaccharides were exhibited mainly by the branched (1 / 3)-b-d-glucan moiety (Sone et al., 1985; Yoshioka, Tabeta, Saito, Uehara, & Fukuoka, 1985). However, the antitumor activities also depend on several factorssolubility in water, size of the molecules, branching rate and its form. The antitumor activity of polysaccharides and their clinical quality can be improved by chemical
modication such as Smith degradation (oxydo-reducto-hydrolysis), formolysis and carboxymethylation (Wasser, 2002). In other study, the crude extracts of Reishi exhibited anticancer activity in in vitro systems against a variety of cancer cells including leukemia, lymphoma, breast, human bladder (Lu et al., 2004), prostate, liver, lung and myeloma cell lines. The mechanism of action include the inhibition of proliferation, induction of apoptosis, induction of cell cycle arrest, inhibition of invasive behavior and suppression of tumor angiogenesis in many experimental systems including prostate cancer (Mahajna et al., 2009). Daba and Ezeronye (2003) had reviewed the anticancer effect of polysaccharides isolated from various higher basidiomycetes mushrooms including Lentinus edodes, Schizophyllum commune and Grifola frondosa. Their review also covered the mode of action of those polysaccharides, the chemical structure as well as some result obtained from the experimental and clinical trails. Latest nding by Hearst et al. (2009) had revealed another benet of mushrooms. Shiitake (Lentinula edodes) and Oyster (P. ostreatus) mushrooms were tested for their antibacterial and antifungal properties. Surprisingly, shiitake extract was found to be effectives as an antimicrobial substance and was signicantly more antibacterial than ciprooxacin. Mushrooms extracts were also reported to exhibit antioxidant properties. Study done by Tsai et al., (2009) has discovered antioxidant properties of P. ostreatus, Pleurotus ferulae and Clitocybe maxima. While Bao, Ushio, and Ohshima (2008) discovered antioxidant properties from Flammulina velutipes. Antioxidant properties of oyster mushrooms (P. ostreatus) were also being studied by Jayakumar, Thomas, and Geraldine (2009). At a maximum concentration of 10 mg/ml, the ethanolic extract of oyster mushroom showed signicant reducing power as compared to commercial antioxidant, the butylated hydroxyl toluene (BHT). This indicates the potential of mushrooms to become a food supplement or even as a pharmaceutical agent. Besides its antibacterial, antimicrobial and antioxidant properties, extract of mushrooms are also potential color stabilizer. Ergothioneine extracted from F. velutipes was able to overcome browning of ground beef and big eye tuna meats (Thunnus obesus) up to 12 and 7 days of storage, respectively. This duration was double and triple to a duration of a controlled storage meats (6 days for ground beef and 2 days for big eye tuna meat), which was not incorporated with the extract (Bao et.al., 2008). Other than its medicinal properties, consumption of edible mushrooms also leads to a signicant health improvement. This is because they are low in calories, sodium, fat and cholesterol, while contain high percentage of protein, carbohydrate, ber, vitamins and minerals. These nutritional properties make mushrooms a very good dietary food, which can contribute to the formulation of a well-balanced diet (Manzi, Gambelli, Marconi, Vivanti, & Pizzoferrato, 1999).
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This has urged an effort from a team of researchers from Johns Hopkins Bloomberg, School of Public Health in Baltimore to investigate the efciency of mushrooms substituting food in controlling weight gain. Their study has shown that substituting ground white button mushrooms for lean ground beef in a single meal for four consecutive days signicantly reduced daily energy and fat intake, without affecting the palatability, appetite, satiation and satiety. One can reduce 1 lb of body fat by just having less than 10 meals. If this substitution constantly made once a week, about 20, 000 kcal or more than 5 lbs can be reduced in a year (Cheskin et al., 2008). Current trends on functional foods In recent years, much attention has been paid to physiological functions of foods due to increasing concerns for health (Arihara, 2006). People have turned to natural food sources such as plants and herbs for these enhancers, rather than articial substances. Increases in consumer demand have resulted in emerging of various health promoting products in the market. They are called dietary supplements, designers foods, super food, nutraceutical as well as functional foods. These terms are actually referred to foods that have special benecial effects on the human (Childs & Poryzees, 1997). There are actually hundreds of denition describing the concept of functional foods. Unfortunately, great variations between various denitions make it difcult to provide industry partners with robust information on market trends and market potential, or to appropriately protect consumers through legislation. These have initiated Doyon and Labrecque (2008) together with a group of experts from North America and Europe to redene the denition of functional foods by using the Delphi technique. Functional food is now dened as food that is, or appears similar to a conventional food. It must be a part of standard diet, which is consumed on regular basis and in normal quantities. Other than that, it should also been proven to reduce the risk of specic chronic diseases or benecially affect target functions beyond its basic nutritional functions. This showed that consumers are more aware on what they eat and drink as they have become more proactive in improving their health. There are a lot of products containing functional ingredients in the marketdinfant milk formulae, bakery products, chocolate, dairy products and health drinks. Prebiotics are among those functional food ingredients which raise much attention recently (Blades, 2000; Roberfroid, 2002; Roberfroid, 2000). A concept of prebiotic Prebiotic oligosaccharides have gain interest in food research area since the last few decades and they are getting more and more attention recently. Prebiotics such as oligosaccharides and inulin have become a great interest as a functional food ingredient because it is able to manipulate the composition of colonic microbiota in human gut by
inhibition of exogenous pathogens (Rycroft, Jones, Gibson, & Rastall, 2001), thus improving the host health (Roberfroid, 2000; Roberfroid, 2002). The term prebiotic was actually introduced by Gibson and Roberfroid (1995), who exchanged pro to pre, which means before or for (Schrezenmeir & Michael, 2001). They dened prebiotics as a non-digestible food ingredient that benecially affects the host by selectively stimulating the growth and/or activity of one or a limited number of bacteria in the colon. They found that the definition of prebiotics is more or less overlaps with the denition of dietary ber, except for its selectivity for certain species. Cummings, Macfarlane, and Englyst (2001) on the other hand had classied prebiotics as those carbohydrates with relatively short chain length. This denition was being updated by Gibson, Probert, Rastall, and Roberfroid (2004) as selectively fermented ingredients that allow specic changes, both in the composition and/or activity in the gastrointestinal microbiota that confers benets upon host well-being and health. Gibson (2004) recognized dietary carbohydrate such as bers as a candidate prebiotics, but oligosaccharide was found to be more promising. Currently available prebiotics such as inulin and its derivatives as well as galacto-oligosaccharides (GOS) are relatively cheap to manufacture and has been widely used as a functional ingredient in food (Macfarlane, Macfarlane, & Cumming, 2006). Examples of some prebiotics and their properties are shown in Table 2. Ingestion of prebiotic was believed to enhance immune function, improve colonic integrity, decrease incidence and duration of intestinal infections, down-regulated allergic response as well as improve digestion and elimination of faeces (Douglas & Sanders, 2008). However, these effects were not the direct consequences upon prebiotic ingestion. Wang (2009) suggested that the effect of prebiotics was actually indirect, because it is the changes in the gastrointestinal microbiota compositions (bidobacterias, lactobacilli, as well as the histolyticum subgroup; bacteroides and clostridia) that give rise to the prebiotics effect. Bidobacteria and lactobacilli are the benecial bacteria that serve as prebiotics target (Macfarlane, Steed, & Macfarlane, 2008). A positive effect of prebiotic reects signicant increase in numbers of bidobacteria and lactobacilli, while retarding the development of histolyticum subgroup (Palframan, Gibson, & Rastall, 2003). Probert and Gibson (2002), Langlands, Hopskin, Coleman, and Cummings (2004) as well as Macfarlane et al. (2006) are among those who reported the increases in number of bidobacteria and lactobacilli in the gut, as a result of prebiotic action. Gibson, Beatty, Wang, and Cumming (1995) found that bidobacteria was able to stimulate the immune system, produce vitamin B, inhibit pathogen growth, reduce blood ammonia and blood cholesterol levels as well as help to restore the normal ora after antibiotic therapy, while the lactobacilli aid digestion of lactose in lactose-intolerant individuals, reduce constipation and infantile
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Coppa, Bruni, Zampini, Galeazzi, & Gabrielli, 2002; Franck, 2002; Roberfroid, 2002; Roberfroid, 2005 LHomme, Arbelot, Puiserver, & Biagini, 2003; Losada & Olleros, 2002 Alander et.al., 2001; Ziegler et.al, 2007 Crittendan & Playne, 1996; Hayakawa et.al., 1990; Jaskari, 1998 Crittendan & Playne, 2002; Yamada, 1993 Macfarlane et al., 2006
diarrhea, help resist infections such as salmonellae and help to relieve irritable bowel syndrome (Manning & Gibson, 2004).
Kaneko, Yokoyama, & Suzuki, 1995; Kohmoto, Fukui, Takaku, & Mitsuoka, 1991
Mushrooms as a potential source of prebiotics Recent developments in prebiotics have heightened the need to search for another potential source of prebiotics. Mushrooms seem to be a potential candidate for prebiotics as it contains carbohydrates like chitin, hemicellulose, band a-glucans, mannans, xylans and galactans (Table 3 simplied ndings on the composition of carbohydrate in mushrooms). Chitin e a water insoluble polysaccharides e accounting up to 80e90% of dry matter in mushroom cell wall, with the N-containing chitin as one of the skeletal fungal polysaccharides that responsible for the rigidity and shape of the wall. Chitin only presents in some taxonomical group of Zygo-, Asco-, Basidio- and Deuteromycetes and does not present in other group like Oomycetes (Vetter, 2007). Manzi, Marconi, Aguzzi, and Pizzoferrato (2004) studied the chitin content in eight samples of Boletus spp. mixtures and found that it ranges from 68 to102 mg/g of dry matter. Chitin molecules were indigestible for human and plays role as a dietary ber (Bauer-Petrovska, Jordanoski, & Kulevanova, 2001; Kalac, 2009 and Cheung, 1996). The bioactivities of water insoluble polysaccharides was however less as compared to water soluble polysaccharides (Tao et al., 2006). This was supported by a study done by Mizuno, Saito, Nishitoba, and Kawagashi (1995) where no antitumor activity of chitin was found. Most of mushrooms polysaccharides present as linear and branched glucans with different types of glycosidic linkages such as (1 / 3), (1 / 6)-b-glucans and (1 / 3)-a-glucans. However, some of them are true heteroglycans containing arabinose, mannose, fucose, galactose, xylose, glucose and glucuronic acids as main side chain components or in different combinations. Even though mushrooms polysaccharides are of different chemical composition, most of them belonging to the group of b-glucans (Wasser, 2002). In Pleurotus spp. it ranges from 2.2 to5.3 mg/g of dry matter, while in Lentinula edodes it was reported to be around 2 mg/g of dry matter as well (Manzi & Pizzoferrato, 2000). In the following year, Manzi, Aguzzi, and Pizzoferrato (2001) revealed the concentration of beta glucan in another three different species of mushrooms including the raw and cooked. Beta glucan in raw A. bisporus was ranging from 1.2 to1.7 mg/g, while in cooked ranging from 0.8 to4.2 mg/g. Raw P. ostreatus and dried Boletus contains 139.2 mg/g and 548.8 mg/g of beta glucan respectively, while the cooked mushroom has slightly higher concentration of beta glucan. Digestive enzymes secreted by the pancreas or brush border of vertebrates, and of mammals in particular, are unable to hydrolyze b-glucosidic bonds. This make them resistant to acid hydrolysis in the stomach and remain non-digestible by human digestive enzymes (Van Loo,
Prebiotics
Inulin
Isomalto-oligosaccharides (IMO)
DP, degree of polymerization; F, fructose; Gal, galactose; G, glucose. Source: Macfarlane et al., 2006; Vernazza, Rabiu, & Gibson, 2006 and Wang, 2009.
References
Commercialized
Commercialized
Commercialized
Commercialized
Status
Commercialized
11e65
2e10
Commercialized
Tranfructosylation from sucrose, or hydrolysis of chicory inulin Produced from lactose by b-galactosidase Extracted from soya bean whey
DP
2e4
Production Method
Oligo-galactose (85%) with some glucose and lactose Mixture of rafnose (F-Gal-G) and stachyose (F-Gal-Gal-G) b(1-4)-linked xylose
b(2-1) fructans
b(2-1) fructans
Composition
Transgalactosylation of maltose
2e8
Commercialized
F.M.N.A. Aida et al. / Trends in Food Science & Technology 20 (2009) 567e575 Table 3. Carbohydrate constituents isolated from various types of mushrooms. Carbohydrate constituents b-glucan Sources Pleurotus ostreatus Pleurotus eryngii Pleurotus tuberregium Ganoderma lucidum Ganoderma lucidum Phellinus baumii Pilat Edible mushrooms in Korea Pleurotus ostreatus, Agaricus bisporus, Flammulina velutipes, Pleurotus eryngii, Lentinus edodes Medicinal mushrooms in Korea Agaricus blazei, Sparassis crispa, Brown rice e Phellinus linteus, Ganoderma lucidum, Inonotus obliquus Krestin Chitin cultured mycelial biomass of Trametes versicolor (Turkey tail) Boletus spp European species of wild mushrooms (Agaricus spp, Boletus spp) fruiting bodies of Lentinus edodes liquid culture broth product of Schizophyllum commune (Split Gill) spores of Ganoderma lucidum Armillaria mellea Wasser, 2002 Manzi et al., 2004 Kalac, 2009 Wasser, 2002 Wasser, 2002 Bao, Liu, et al., 2001; Bao, Duan, et al.,2001 Sun, Liang, Zhang, Tong, & Liu, 2009 Revealed by
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Water-soluble heteropolysaccharides constituted with D-galactose, D-mannose, D-xylose, L-fructose, L-(or D)-arabinose Xylose, Fructose, Mannose, Glucose, Sucrose, Trehalose
Yoshioka et al., 1985; Synytsya et al., 2008; Tong et.al., 2009 Synytsya et al., 2008 Tao et al., 2006 Wang & Zhang, 2009 Sone et al., 1985; Miyazaki, 1982; Ge, Zhang & Sun, 2009 Kim et al., 2009
Lentinan Schizophyllan (1 / 3)-a-d-glucan and b-(1 / 3)-linked glucans Water soluble polysaccharides; (1 / 6) -linked-a-d-glucopyranosyl, (1 / 2,6)-linked-a-d-glucopyranosyl, (1 / 6)-linked-a-d-galactopyranosyl
2006). The non-digestible property of mushroom carbohydrate enables it to be considered as a potential source of prebiotic, as it meets part of prebiotics denition. However, intense studies need to be carried out, before such claim could be made because not all dietary carbohydrates are prebiotics (Gibson et al., 2004). Synytsya et al. (2008) gave a positive overview that mushrooms extract of P. ostreatus and P. eryngii were able to stimulate the growth of probitics e Lactobacillus ssp. (4 strains: Lac AeD), Bidobacterium ssp.(3 strains: Bi AeC) and Enterococcus faecium (2 strains: Ent A and B) e to some extent. Maximum growth rate, maximum biomass concentration and nal acid production were observed in the study. It was found that extract from P. eryngi support the growth of Lactobacillus strains better than P. ostreatus. Lactobacillus B and C showed the highest production of short chain fatty acid (SCFA), while Bidobacteria A showed the lowest amount of SCFA when supplemented with both extracts. Wang (2009) has highlighted and pointed out the important criteria of prebiotics. Fig. 1 illustrated the criteria for
classication of a food ingredient in order to be regarded as prebiotic. The rst criteria for prebiotics, which is nondigestible or resistant to upper gut tract is actually to ensure that the prebiotics can withstand digestive processes before they reach the colon, thus stimulate the benecial bacteria; bidobacteria and lactobacilli effectively (Gibson & Collins, 1999; Macfarlane et al., 2008). Resistance to digestive processes includes resistance towards gastric acidity, hydrolysis by mammalian enzymes and gastrointestinal absorption (Gibson et al., 2004). Some of the non-digestible oligosaccharides presently available or in development as food ingredients include carbohydrates in which the monosaccharide unit is fructose, galactose, glucose and/or xylose. The non-digestible oligosaccharides are made of one, two or even three monosachharides and have no nutritional signicant (Quigley, Hudson, & Englyst, 1999; Roberfroid, 2000). It is water soluble and exhibits some sweetness. However, the degree of sweetness depends on the chain length. It was reported that inulin with degree of polymerization more than ten does not taste sweet anymore (Roberfroid, 2000).
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Prebiotics Criteria
Fig. 1. Criteria for classication of a food ingredient as prebiotic. (Source: Wang, 2009).
Criteria which allow the classication of a food ingredient as a prebiotic also include selective fermentation by potentially benecial bacteria in the colon (Gibson et al., 2004; Wang, 2009). The effects of this fermentation may lead to an increase in the expression or change in the composition of short-chain fatty acids, increased fecal weight, a mild reduction in luminal colon pH, a decrease in nitrogenous end products and reductive enzymes, an increased expression of the binding proteins or active carriers associated with mineral absorption and immune system modulation (Douglas & Sanders, 2008), which is benecial to the host health; requirement for the third criteria. Selective stimulation of the growth and/or activity of intestinal bacteria potentially associated with health and well-being is considered as one of the criteria of prebiotics (Gibson et al., 2004). Prebiotics are reported to be particularly suited to the growth and activities of probiotics, bidobacteria and lactobacilli (Wang, 2009) and suppress the growth of clostridia and bacteroides. Palframan et al. (2003) had came out with a comparative quantitative tool known as Prebiotic Index (PI) for measurement of prebiotic effects in vitro. Assumption from the equation is that the increases in the population of bidobacteria and/or lactobacilli are considered a positive effect, while an increase in bacteroides and clostridia (histolyticum subgroup) are negative. PI can be calculated using the following equation: Prebiotic Index Bif Bac Lac Clos Total Total Total Total
compared to the rest. Inulin alone however showed negative PI at 8 h, but a positive PI at 24 h. However, this is the toughest criteria to be fullled. Not all candidate prebiotics showed selective fermentation. Study conducted by Langlands et al. (2004) and Duncan, Scott, and Ramsay (2003) demonstrated that fermentation of prebiotics-inulin has caused an increased in other bacterial genera such as Roseburia, Ruminococcus and Eubacterium in the gut. This is because different people harbour different bacterial species and the composition of the microbiota can be affected by a variety of other factors such as diet, disease, drugs, antibiotic, age and others (Macfarlane et al., 2006). Last but not least, a prebiotic must be able to withstand food processing conditions so that they remain intactdnot degraded or chemically altereddand available for bacterial metabolism in gut Huebner, Wehling, Parkhurst, and Hutkins (2008). As a result, the gastrointestinal health of human can be improved (Tuohy, Probert, Smejkal, & Gibson, 2003). Huebner et al. (2008) has tested a few commercial prebiotics over several processing conditions. It has conclusively shown that only heating at low pH caused signicant reduction in prebiotic activity of inulin, while fructooligosaccharides (FOS) contained product was observed to be the least stable. Other processing condition testeddprocessing at low pH and Maillard reaction conditiondshowed minimum changes in prebiotic activity. Conclusions The roles of prebiotic in improving and maintaining human health have been studied extensively. Food containing prebiotics can now be found easily in the market. These include bread, cereal bar, spread, confectioneries, sauces, infant milk formulae, beverages and health drink. Developing a new potential prebiotic from inexpensive and abundant materials like mushrooms are those qualities that need to be considered. There are great advantages of incorporating the mushrooms extracts in food as its polysaccharides were reported to exhibit immunomodulating properties, antitumor activities as well as anticancer activities. Consumers will not only beneted with the prebiotic effect of mushrooms extract, but also enjoying the medicinal benet of it. Even though scientic experiments have proven
Where Bif is bidobacterial numbers at sample time/numbers at inoculation, Bac is bacteroides numbers at sample time/numbers at inoculation, Lac is lactobacilli numbers at sample time/numbers at inoculation, Clos is Clostridia numbers at sample time/numbers at inoculation and total is total bacteria numbers at sample time/numbers at inoculation. Ghoddusi, Grandison, Grandison, and Tuohy (2007) studied the prebiotic effect of several candidate prebiotics-inulin, fructooligosaccharides, polydextrose and isomaltooligosaccharides alone and in combinationdby using Prebiotic Index. Mixture of fructooligosaccharides and inulin showed the highest PI at 8 h and 24 h as
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a signicant prebiotic effect of P. ostreatus and Pleurotus eryngii on selective microorganisms, an intensive and more thorough research need to be conducted as other prebiotic criteria has not been conrmed. It needs to be supported with thorough in vivo and in vitro studies. Furthermore, the avor of mushrooms extract need to be further studied and evaluated as it may impart the sensory properties of nal product. To date, only compounds responsible for the avor of mushrooms have being published and no reported data was found on the avor of extracted polysaccharides from mushrooms. Those ndings however reect a great potential of mushroom to be regarded as a source of prebiotics.
References
Alander, M., Mattao, J., Kneifel, W., Johansson, M., Kogler, B., Crittenden, R. G., et al. (2001). Effect of galacto-oligosaccharide supplementation on human faecal microora and on survival and persistence of Bidobacterium lactis Bb-12 in the gastrointestinal tract. International Dairy Journal, 11, 817e825. Arihara, K. (2006). Strategies for designing novel functional meat products. Meat Science, 74, 219e229. Bao, H. N. D., Ushio, H., & Ohshima, T. (2008). Antioxidative activity and antidiscoloration efcacy of ergothioneine in mushroom (Flammulina velutipes) extract added to beef and sh meats. Journal of Agricultural and Food Chemistry, 56, 10032e10040. Bao, X., Duan, J., Fang, X., & Fang, J. (2001). Chemical modication of the (1 / 3)-a-D-glucan from spore of Ganoderma lucidum and an investigation of their physicochemical properties and immunological activity. Carbohydrate Research, 336, 127e140. Bao, X., Liu, C., Fang, J., & Li, X. (2001). Structural and immunological studies of a major spores of Ganoderma lucidum (Fr.) Karst. Carbohydrate Research, 332, 67e74. Bauer-Petrovska, B., Jordanoski, V., & Kulevanova, S. (2001). Investigation of dietary bre in some edible mushrooms from Macedonia. Nutrition and Food Science, 31, 242e246. Blades, M. (2000). Functional foods or nutaceuticals. Journal of Nutrition and Food Science, 30(2), 73e75. Chang, S. T. (1999). Global impact of edible and medicinal mushrooms on human welfare in the 21st century: non-green revolution. International Journal of Medicinal Mushrooms, 1, 1e7. Chang, S. T. (2001). Products of medicinal mushrooms as a good source of dietary supplements. Retrieved 15 February, 2009, from. http://www.isms.biz Cheskin, L. J., Davis, L. M., Lipsky, L. M., Mitola, A. H., Lycan, T., Mitchell, V., et al. (2008). Lack of energy compensation over 4 days when white button mushrooms are substituted for beef. Appetite, 51, 50e57. Cheung, P. C. K. (1996). Dietary ber content and composition of some cultivated edible mushroom fruiting bodies and mycelia. Journal of Agricultural and Food Chemistry, 44, 468e471. Childs, N. M., & Poryzees, G. H. (1997). Foods that help prevent disease: consumer attitudes and public policy implications. British Food Journal, 9, 419e426. Coppa, G. V., Bruni, S., Zampini, L., Galeazzi, T., & Gabrielli, O. (2002). Prebiotics in infant formulas: Biochemical characterisation by thin layer chromatography and high performance anion exchange chromatography. Digestive and Liver Disease, 34, 124e 128. Crittendan, R. G., & Playne, M. J. (1996). Production, properties and applications of food-grade oligosaccharides. Trends in Food Science & Technology, 7, 353e361.
Crittendan, R. G., & Playne, M. J. (2002). Purication of food-grade oligosaccharides using immobilized cells of Zymomonas mobilis. Applied Microbiology and Biotechnology, 58, 297e302. Cummings, J. H., Macfarlane, G. T., & Englyst, H. N. (2001). Prebiotic digestion and fermentation. American Journal of Clinical Nutrition, 73(Suppl.), 415e420. Daba, A. S., & Ezeronye, O. U. (2003). Anti-cancer effect of polysaccharides isolated from higher basidiomycetes mushrooms. African Journal of Biotechnology, 2(2), 672e678. Douglas, L. C., & Sanders, M. E. (2008). Probiotics and prebiotics in dietetics practice. Journal of the American Dietetic Association, 108, 510e521. Doyon, M., & Labrecque, J. A. (2008). Functional foods: a conceptual denition. British Food Journal, 110(11), 1133e1149. Duncan, S. H., Scott, K. P., & Ramsay, A. G. (2003). Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Applied Enviromental Microbiology, 69, 1136e1142. FAO. (2009). Food & Agriculture Organization of the United Nations. Retrieved 15 February 2009, from. http://www.fao.org/corp/statistics/en Franck, A. (2002). Technological functionality of inulin and oligofructose. British Journal of Nutrition, 87, 287e291. Ge, Q., Zhang, A. Q., & Sun, P. L. (2009). Structural investigation of a novel water-soluble heteropolysaccharide from the fruiting bodies of Phellinus baumii Pilat. Food Chemistry, 114, 391e395. Ghoddusi, H. B., Grandison, M. A., Grandison, A. S., & Tuohy, K. M. (2007). In-vitro study on gas generation and prebiotic effects of some carbohydrates and their mixtures. Anaerobe, 13, 193e199. Gibson, G. R. (2004). From probiotics to prebiotics and healthy digestive system. Journal of Food Science, 69(5), 141e143. Gibson, G. R., Beatty, E. R., Wang, X., & Cumming, J. H. (1995). Selective stimulation of bidobacteria in the human colon by oligofructose and inulin. Gastroenterology, 108, 975e982. Gibson, G. R., & Collins, M. (1999). Concepts of balanced colonic microbiota, prebiotics and synbiotics. In L. A. Hanson, & R. H. Yolken (Eds.), Probiotics: Other nutritional factors and intestinal microora. Philadelphia: Raven Publishers. Gibson, G. R., & Roberfroid, M. B. (1995). Dietary modulation of the human colonic microbiota. Introducing the concept of prebiotics. Nutrition, 125, 1401e1412. Gibson, G. R., Probert, H. M., Rastall, R. A., & Roberfroid, M. B. (2004). Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutrition Research Reviews, 17, 259e275. Hayakawa, K., Mitzuni, J., Wada, K., Masai, T., Yoshihara, I., & Mitsuoka, T. (1990). Effect of soybean oligosaccharides on human faecal ora. Microbial Ecology in Health and Disease, 3, 293e303. Hearst, R., Nelson, D., McCollum, G., Millar, B. C., Maeda, Y., Goldsmith, C. E., et al. (2009). An examination of antibacterial and antifungal properties of constituents of Shiitake (Lentinula edodes) and Oyster (Pleurotus ostreatus) mushrooms. Complementary Therapies in Clinical Practice, 15, 5e7. Huebner, J., Wehling, R. L., Parkhurst, A., & Hutkins, R. W. (2008). Effect of processing conditions on the prebiotic activity of commercial prebiotics. International Dairy Journal, 18, 287e293. Jaskari, J. (1998). Oat beta-glucan and xylan hydrolyzates as selestive substrates for Bidobacterium and Lactobacillus strains. Applied Microbiology and Biotechnology, 49, 75e181. Jayakumar, T., Thomas, P. A., & Geraldine, P. (2009). In-vitro antioxidant activities of an ethanolic extract of the oyster mushroom (Pleurotus ostreatus). Innovative Food Science and Emerging Technologies, 10, 228e234. Kaneko, T., Yokoyama, A., & Suzuki, M. (1995). Digestibility charaqcteristics of isomaltooligosaccharides in comparison with several saccharides using the rat jejunum loop method. Bioscience, Biotechnology and Biochemistry, 59, 1190e1194.
574
F.M.N.A. Aida et al. / Trends in Food Science & Technology 20 (2009) 567e575 Probert, H. M., & Gibson, G. R. (2002). Investigating the prebiotic and gas generating effects of selected carbohydrates on the human colonic microora. Letters in Applied Microbiology, 35, 473e480. Quigley, M., Hudson, G. J., & Englyst, H. N. (1999). Determination of resistant short chain carbohydrates (non-digestible oligosaccharides) using gas-liquid chromatography. Food Chemistry, 65, 381e 390. Roberfroid, M. (2002). Functional food concept and its application to prebiotics. Digest Liver, 34(Suppl. 2), 105e110. Roberfroid, M. B. (2000). Chicory fructooligosaccharides and the gastrointestinal tract. Nutrition, 16(7/8), 677e679. Roberfroid, M. B. (2005). Inulin-type fructans as functional food ingredients. Boca Rotan: CRC Press. Rycroft, C. E., Jones, M. R., Gibson, G. R., & Rastall, R. A. (2001). A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. Journal of Applied Microbiology, 91, 878e887. Sanchez, C. (2004). Mini-review: modern aspects of mushroom culture technology. Applied Microbiology and Biotechnology, 64, 756e762. Schrezenmeir, J., & Michael, V. (2001). Probiotics, prebiotics and synbiotics e approaching a denition. American Journal of Clinical Nutrition, 73(Suppl.), 361e364. Sone, Y., Okuda, R., Wada, N., Kishida, E., & Misaki, A. (1985). Structures and antitumor activities of the polysaccharides isolated from fruiting body and the growing culture of mycelium of Ganoderma lucidum. Agricultural and Biological Chemistry, 49(9), 2641e2653. Sun, Y., Liang, H., Zhang, X., Tong, H., & Liu, J. (2009). Structural elucidation and immunological activity of a polysaccharide from the fruiting body of Armillaria mellea. Bioresource Technology, 100, 1860e1863. Synytsya, A., Mickova, K., Synytsya, A., Jablonsky, I., Spevacek, J., Erban, V., et al. (2008). Glucans from fruit bodies of cultivated mushrooms Pleurotus ostreatus and Pleurotus eryngii: structure and potential prebiotic activity. Carbohydrate Polymers. doi:10.1016/ j.carbpol.2008.11.021. Tao, Y., Zhang, L., & Cheung, P. C. K. (2006). Physicochemical properties and antitummor activities of water-soluble native and sulfated hyperbranched mushroom polysaccharides. Carbohydrate Research, 341, 2261e2269. Tong, H., Xia, F., Feng, K., Sun, G., Gao, X., Sun, L., et al. (2009). Structural characterization and in vitro antitumor activity of a novel polysaccharide isolated from the fruiting bodies of Pleurotus ostreatus. Bioresource Technology, 100, 1682e1686. Tsai, S. Y., Huang, S. J., Lo, S. H., Wu, T. P., Lian, P. Y., & Mau, J. L. (2009). Flavour components and antioxidant properties of several cultivated mushrooms. Food Chemistry, 113, 578e 584. Tuohy, K. M., Probert, H. M., Smejkal, C. W., & Gibson, G. R. (2003). Using probiotics and prebiotics to improve gut health. Drug Discovery Today, 8(15), 692e700. Van Loo, J. (2006). Inulin-type fructans as prebiotics. In G. R. Gibson, & R. A. Rastall (Eds.), Prebiotics: Development and application (pp. 59). Hoboken, NJ: John Wiley & Sons. Vernazza, C. L., Rabiu, B. A., & Gibson, G. R. (2006). Human colonic microbiology and the role of dietary intervention: introduction to prebiotics. In G. R. Gibson, & R. A. Rastall (Eds.), Prebiotics: Development and application. Hoboken, NJ: John Wiley & Sons. Vetter, J. (2007). Chitin content of cultivated mushrooms Agaricus bisporus, Pleurotus ostreatus and Lentinula edodes. Food Chemistry, 102, 6e9. Wang, Y. (2009). Prebiotics: present and future in food science and technology. Food Research International, 42, 8e12.
Kalac, P. (2009). Chemical composition and nutritional value of European species of wild growing mushrooms: a review. Food Chemistry, 113, 9e16. Kim, H. S., Kacew, S., & Lee, B. M. (1999). In-vitro chemopreventive effects of plant polysaccharides (Aloe barbandensis Miller, Ganoderma lucidum and Coriolus versicolor). Carcinogenesis, 20(8), 1637e1640. Kim, M. Y., Chung, M., Lee, S. J., Ahn, J. K., Kim, E. H., Kim, M. J., et al. (2009). Comparison of free amino acid, carbohydrates concentrations in Korean edible and medicinal mushrooms. Food Chemistry, 113, 386e393. Kohmoto, T., Fukui, F., Takaku, H., & Mitsuoka, T. (1991). Dose response test of isomaltooligosaccharides for increasing faecal bidobacteria. Agricultural and Biological Chemistry, 55, 2157e 2159. Kues, U., & Liu, Y. (2000). Fruiting body production in basidiomycetes. Application Microbiology and Biotechnology, 54, 141e152. Langlands, S. J., Hopskin, M. J., Coleman, N., & Cummings, J. H. (2004). Prebiotic carbohydrates modify the mucosa-associated microora of the human large bowel. Gut, 53, 1610e1616. LHomme, C., Arbelot, M., Puiserver, A., & Biagini, A. (2003). Kinetics of hydrolysis of fructooligosaccharides in mineral-buffered aqueous solutions: Inuence of pH and temperature. Journal of Agricultural and Food Chemistry, 51, 224e228. Liu, X., Yuan, J. P., Chung, C. K., & Chen, X. J. (2002). Antitumor activity of the sporederm-broken germinating spores of Ganoderma lucidum. Cancer Letters, 182, 155e161. Losada, M. A., & Olleros, T. (2002). Towards a healthier diet for the colon: the inuence of fructooligosaccharides and Lactobacilli on intestinal health. Nutrition Research, 22, 71e84. Lu, Q. Y., Jin, Y. S., Zhang, Q., Zhang, Z., Heber, D., Go, V. L. W., et al. (2004). Ganoderma lucidum extracts inhibit growth and induce actin polymerization in bladder cancer cells in vitro. Cancer Letters, 216, 9e20. Macfarlane, G. T., Steed, H., & Macfarlane, S. (2008). Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. Journal of Applied Microbiology, 104, 305e 344. Macfarlane, S., Macfarlane, G. T., & Cumming, J. H. (2006). Review article: prebiotics in the gastrointestinal tract. Alimentary Pharmacology and Therapeutics, 24, 701e714. Mahajna, J., Dotan, N., Zaidman, B. Z., Petrova, R. D., & Wasser, S. P. (2009). Pharmacological values of medicinal mushrooms for prostate cancer therapy: the case of Ganoderma lucidum. Nutrition and Cancer, 61(1), 16e26. Manning, T. S., & Gibson, G. R. (2004). Prebiotics. Best Practice & Research Clinical Gastroenterology, 18, 287e298. Manzi, P., Aguzzi, A., & Pizzoferrato, L. (2001). Nutritional value of mushrooms widely consumed in Italy. Food Chemistry, 73, 321e325. Manzi, P., Gambelli, L., Marconi, S., Vivanti, V., & Pizzoferrato, L. (1999). Nutrients in edible mushrooms: an inter-species comparative study. Food Chemistry, 65, 477e482. Manzi, P., Marconi, P., Aguzzi, A., & Pizzoferrato, L. (2004). Commercial mushrooms: nutritional quality and effect of cooking. Food Chemistry, 84, 201e206. Manzi, P., & Pizzoferrato, L. (2000). Beta-glucans in edible mushrooms. Food Chemistry, 68, 315e318. Miyazaki, T. (1982). Structural examination of an alkali-extracted, water-soluble heteroglycan of the fungus. Carbohydrate Research, 109, 290e294. Mizuno, T., Saito, H., Nishitoba, T., & Kawagashi, H. (1995). Antitumor active substances from mushrooms. Food Review International, 11, 23e61. Palframan, R., Gibson, G. R., & Rastall, R. A. (2003). Development of a quantitative tool for comparison of the prebiotic effect of dietary oligosaccharides. Letters in Applied Microbiology, 37, 281e284.
F.M.N.A. Aida et al. / Trends in Food Science & Technology 20 (2009) 567e575 Wang, J., & Zhang, L. (2009). Structure and chain conformation of ve water-soluble derivatives of a b-D-glucan isolated from Ganoderma lucidum. Carbohydrate Research, 344, 105e112. Wasser, S. P. (2002). Medicinal mushrooms as a source of antitumor and immonomudulating polysaccharides. Applied Microbiology and Biotechnology, 60, 258e274. Yamada, H. (1993). Structure and properties of oligosaccharides from wheat bran. Cereal Foods World, 38, 490e492.
575
Yoshioka, Y., Tabeta, R., Saito, H., Uehara, N., & Fukuoka, F. (1985). Antitumor polysaccharides from P. ostreatus (FR) Quel.: isolation and structure of a b-glucan. Carbohydrate Research, 140, 93e100. Ziegler, E., Vanderhoof, J. A., Petchow, B., Mitmesser, S. H., Stolz, S. I., Harris, C. L., et al. (2007). Term infants fed formula supplemented with selected blends of prebiotics grow normally and have stools similar to those reported for breast-fed infants. Journal of Pediatric Gastroenterology and Nutrition, 44, 359e364.