|Year : 2021 | Volume
| Issue : 4 | Page : 335-339
Fermented foods as probiotics: A review
Yulistia Budianti Soemarie1, Tiana Milanda2, Melisa Intan Barliana3
1 Department of Biological Pharmacy, Faculty of Pharmacy, Universitas Padjadjaran, West Java; Departement of Biological Pharmacy, Faculty of Pharmacy, Islam Kalimantan Muhammad Arsyad Al Banjari University, Banjarmasin City, South Borneo, Indonesia
2 Department of Biological Pharmacy, Faculty of Pharmacy, Universitas Padjadjaran, West Java, Indonesia
3 Department of Biological Pharmacy, Faculty of Pharmacy, Universitas Padjadjaran, West Java; Centre of Excellent in Higher Education for Pharmaceutical Care Innovation, Padjadjaran University, Bandung, Indonesia
|Date of Submission||30-Apr-2021|
|Date of Decision||05-Jun-2021|
|Date of Acceptance||08-Jun-2021|
|Date of Web Publication||20-Oct-2021|
Dr. Tiana Milanda
Departement of Biological Pharmacy, Faculty of Pharmacy, Padjadjaran University, Jl. Raya Jatinangor, Hegarmanah, Kec. Jatinangor, Kab. Sumedang, West Java
Source of Support: None, Conflict of Interest: None
Fermented foods and drinks derived from animals as well as plants play an important role in diets. These foods usually contain lactic acid bacteria (LAB) grown during fermentation, and these naturally contain compounds, including organic acids, ethanol, or antimicrobial compounds with the ability to inhibit spoilage organisms and pathogenic bacteria in fermented foods. Furthermore, these bacteria are able to adapt well to the spontaneous fermentation process and play a role in human as well as animal health, especially in digestive tract, commonly known as probiotics. This study therefore aims to describe the microorganisms produced by fermented foods suitable for development as probiotics to improve human health, as these generally have the ability to improve the immune system against pathogenic bacteria. Several genera are used as probiotics, including Lactobacillus, Bifidobacterium, Bacillus, Pediococcus, and several yeasts. Therefore, LAB produced from fermented foods were concluded to be suitable potential candidates for probiotics, to replace antibiotics in overcoming pathogenic bacteria, and to possess the ability to improve the immune system and strengthen the body against pathogenic bacteria.
Keywords: Fermented foods, lactic acid bacteria, probiotics
|How to cite this article:|
Soemarie YB, Milanda T, Barliana MI. Fermented foods as probiotics: A review. J Adv Pharm Technol Res 2021;12:335-9
| Introduction|| |
Fermented foods have been a major part of human diet for centuries. Furthermore, fermented foods derived from meat, milk, and plant foods have a longer shelf-life, compared to fresh raw materials. This is because fresh foods are very perishable due to their high water content and nutritional value. Fermented foods and drinks derived from animals and plants play an important dietary role in various parts of the world including Asia as well as western countries, and contain nutrients with great potential in maintaining health and preventing disease, but also undergo changes in taste, texture, decreased toxicity, and cooking time., These foods naturally contain compounds, including organic acids, ethanol, or antimicrobial compounds, with the ability to inhibit any spoilage organisms and pathogenic bacteria present.
LAB were initially isolated from fermented food but are the most suitable candidate for increasing fermentation, in terms of product safety, and also have the ability to spontaneously adapt well during the fermentation process. Recently, the role of bacteria in human and animal health has begun to develop quite well, especially in terms of the digestive tract and protection against disease. Lactic acid bacteria (LAB) isolated from fermented foods with the ability to aid in digestive health are known as probiotics, and are generally used as microbe-containing dietary supplements, as well as considered as an important functional food group. Thus, consuming probiotics is useful for maintaining health against pathogenic bacteria in the gut microbiota, and maintaining the normal balance of gut microbiota helps to improve digestive health as well as the immune system.
| Fermentation|| |
Fermentation is known as one of the oldest food preservation methods in the world, and is also a food processing technique to reduce or even eliminate toxic compounds present. A previous study utilized various microorganism types to convert starch into protein by inserting inorganic nitrogen. In general, fermentation generally occurs in the presence of fungi or bacteria, and in this process, microorganisms produce several compounds, including organic acids, gas (alcohol), carbon dioxide, diacetyl, hydrogen peroxide, phenylacetic acid, bacteriocins, and peptides. This process is aimed at extending the shelf life of fruits, vegetables, meat, and fish, and also serves the main roles of food preservation through the formation of metabolites with the ability to inhibit pathogenic or spoilage bacteria, for instance, organic acids (lactic acid, acetic acid, formic acid, and propionic acid), ethanol, carbon dioxide, diacetyl, reuterin, bacteriocins, and others, often associated with water reduction due to the addition of a sufficiently large salt quantity.
| Microorganisms Role in the Fermentation Process|| |
The fermentation of food products utilizes LAB, and several other bacteria, for instance, pathogens, as well as yeast and mold. LAB occur naturally in food, especially fermented products, and play an important role in almost all food and beverage fermentation processes. These bacteria also produce organic acids with the ability to extend the shelf life of fermentation products, and are naturally found in soil, water, manure, waste, and plants, as well as parts of the mucous membrane, including human and animal intestines, mouth, skin, urinary tract as well as genitals, and probably, have a beneficial effect on these organs. After discovery, LAB gained numerous benefits in various applications, for instance, as starters in food and feed fermentation, pharmaceuticals, probiotics, and biological control agents. Taxonomically, these bacteria are divided into two different phyla, Firmicutes and Actinobacteria. Phylum Firmicutes comprises Lactobacillus, Lactococcus, Leuconostoc, Oenococcus, Pediococcus, Streptococcus, Enterococcus, Tetragenococcus, Aerococcus, Carnobacterium, Weissella, Alloiococcus, Symbiobacterium and Vagococcus genuses and Actinobacteria consist of Atopobium and Bifidobacterium.
| Fermented Foods in Different Countries as a Source of Lactic Acid Bacteria|| |
Brem (Bali, Indonesia)
This is a traditional food made of white glutinous rice originating from Indonesia, produced precisely from glutinous rice extract, with a sweet and sour taste, starchy texture, and is usually consumed as a snack. Furthermore, the food has two variants, solid white and yellowish-white, as well as liquid brem produced from rice wine. The production of solid brem involves fermentation of glutinous rice using yeast, while the liquid counterpart does not involve yeast. Furthermore, the food is believed to be good for skin health, warming the body as well as increasing appetite.
This is a fermented product originating from Indonesia, especially Bangka and Lampung, usually produced by adding a lot of salt (10%–25% composition), as well as sugar or rice (10%), to fermented fish, followed by anaerobic fermentation for about 14 days. The addition of over 10% salt prevents the growth of pathogenic bacteria, with the ability to accelerate putrefaction and cause a sour taste. In addition, the final product of rusip contains Streptococcus, Lactobacillus, and Leuconostoc LAB.
This is a traditional fermented vegetable originating from Korea, fermented at 15°C for ± 1 week, or at 25°C for ± 3 days. However, the lowest possible temperature is preferred for manufacture because this prevents the food from being overcooked, having an overly sour taste, and also keeps the taste optimal during a long shelf life. Kimchi is made from a combination of Chinese cabbage (baechu), onions, radishes, chili powder, and garlic as well as several other foods, for instance, carrots, apples, pears, or shrimp. The food also contains several bacteria groups, including LAB (Lactobacillus, Leuconostoc, and Weissella) and pathogenic bacteria (Pseudomonas and Pantoea).
Gochujang is made using chili powder, glutinous rice powder, soy porridge with salt, flavorings, for instance, shallots and garlic, as well as sweetener in the form of sugar syrup, and the mixture fermented for a long time. Subsequently, the microorganisms formed during the fermentation process including, Zygosaccharomyces and Candida, Bacillus velezencis as well as Oceanobacillus obtain protein and carbohydrate intake from the glutinous rice powder and soybean porridge present.
Kefir is produced by nonspontaneous fermentation because a starter culture in the form of lactose symbiotic fermented yeast, for instance, Kluyveromyces marxianus and or non-lactose fermented yeast, for instance, Saccharomyces cerevisiae, must be added prior to the process. In addition, several studies on Kefir showed various species of LAB, pathogenic bacteria, and yeast, including Lactococcus lactis subsp. lactis, Streptococcus thermophilus, Lactobacillus delbureckii subsp. bulgaricus, Lactobacillus helveticus, Lactobacillus casei subsp. pseudoplantarum, Lactobacillus brevis, Lactobacillus paracasei, Lactobacillus kefiranofaciens, Lactobacillus plantarum, Lactobacillus kefiri, Acetobacter lovaniensis, Acetobacter orientalis, S. cerevisiae, S. unisporus, Candida kefyr, K. marxianus, and Leuconostoc mesenteroide.,,
Gundruk is produced from fresh local vegetables, for instance, rayosag (Brassica rapa subsp. Campestris var. Cuneifolia), cabbage (Brassica sp.), mustard leaves (Brassica juncea (L.) Czern), and cauliflower leaves (Brassica oleracea L. var. botrytis L.). The vegetables are withered for 1–2 days, finely crushed, pressed in an airtight container, fermented naturally for about 15–22 days, then sun-dried for 2–4 days. Several LAB including Pediococcus pentosaceus, Lactobacillus fermentum, L. plantarum, L. casei, and L. casei subsp. pseudoplantarum have been found in Gundruk.
This is a pickled cucumber (Cucumis sativus L.) snack originating from Nepal, usually processed with a combination of salt, mustard, and chili powder, then fermented at room temperature, for approximately 7 days. Khalpi is produced using cucumber alone or combined with bacteria, for instance, L. plantarum, L. brevis, Leuconoctoc fallax, and S. cerevisiae. The cucumber is cut, dried for 2 days, then placed in an airtight container, and fermented for 3–5 days.
This is an alcoholic beverage produced by the fermentation of grape juice. The word “wine” is derived from a type of fruit often fermented to produce this drink. The beverage's stability is greatly influenced by the pH factor, a value approaching neutral (pH 7) that makes all microbes and yeast types more active for fermentation and even decay. Meanwhile, a value below 3.5 inhibits the growth of most microbes; thus, only a few microbes are able to participate in fermentation. Furthermore, the fermentation of grapes to produce wine usually requires the aid of bacterial culture, including Staphylococcus cerevisiae, used for the process of converting sugars present in grape juice into alcohol compounds and organic acids. These, in turn, form aldehydes, esters, and other chemical compounds, to extend shelf-life.
Garris is produced by mixing camel milk with some black cumin seeds (Nigella Sativa) and an onion, and is fermented with the help of organisms, including Lactobacillus and yeast. Compared to cow milk, camel milk has a longer shelf-life, and does not rot quickly, even in hot conditions. Furthermore, majority (about 50%) of the identified LAB present in Garris are Streptococcus Lactis subsp. Diacetylactis, while the other bacteria identified are Lactobacillus sp. (L. plantarum, L. casei, L. brevis, Lactobacillus leichmannii, L. fermentum, and Lactobacillus acidophilus).
This is fermented milk, similar to yogurt, originating from Ethiopia, and produced by spontaneous fermentation or without the addition of a starter culture. Ergo is milky white, thick, with great smell and taste, as well as a 15–20 day shelf-life. Several microbes including aerobic mesophilic bacteria, LAB, Staphylococcus and yeast have been identified in this food. Furthermore, several studies have shown Ergo fermentation produces several genera of LAB including, Lactobacillus, Leuconostoc, Enterococcus, Lactococcus, and Streptococcus. Micrococcus, coliform, and spore species are also present in this fermentation process. A reduction in pH leads to the formation of antimicrobial compounds in the food, and consequently, a reduction in the number of microbes present. Lactococcus sp. is the most dominant species in the Ergo fermentation process, having up to 109 cfu/ml colonies until the process' end. Meanwhile, mesophilic bacteria also showed a similar value, and yeast showed an increase in colony number of up to 105 cfu/ml, for 24 h.
| Role of Microorganisms as Probiotics|| |
The term “probiotics” refers to microorganisms providing benefits to humans as well as animals, with a role in the intestinal microbe balance and an important role in health maintenance. These microorganisms often come from the genus Lactobacillus and Bifidobacterium but also come from the genus Bacillus, Pediococcus as well as some yeasts. The genus Lactobacillus is a heterogeneous group of LAB as well as the most widely used bacteria in food and feed fermentation, in addition to being widely used in the manufacture of probiotics. Furthermore, Lactobacillus are Gram-positive bacteria producing the final product in the form of lactic acid, during fermentation.
Analyses on probiotic microbial strains are conducted in vitro and in vivo. Several in vitro analyses include testing for antibiotic resistance profiles, bacteria's origin, and safety evaluation in terms of virulence associated with pathogenic bacteria. Furthermore, probiotic microbial strains ought to be tested in relation to strain adherence to intestinal epithelial cells, intestinal mucosal permeability, and immunomodulatory effects., In this study, in vivo analysis was performed out using experimental animals, for example, Rattus norvegicus or albino strains.
Probiotic bacterial strains are applicable to several food products, for instance, yogurt with Lactobacillus reuteri and Lactobacillus rhamnosus bacteria, fermented milk complete with inulin from strains of Bifidobacterium animalis and L. acidophilus, chocolate products with strains of L. paracasei and condensed milk with L. acidophilus. In addition, these strains are also utilized in improving the health of the human body both directly and indirectly, including defense against the mucosa, repair of normal microflora, preventing infection, defense against food allergies, lowering blood cholesterol levels, cariogenic activity, modulating the mucosal immune system, enhancing the system digestion, as well as maintaining the intestinal microflora balance.
| Conclusion|| |
LAB have an important role in food fermentation due to the ability to produce compounds good for improving human and animal health. Furthermore, LAB produced from single or mixed cultures derived from fermented foods are suitable probiotics for improving digestive tract by maintaining the balance of gut microbiota. These microorganisms also have the capacity to improve the immune system against pathogenic bacteria. Several genera are used as probiotics, including Lactobacillus, Bifidobacterium, Bacillus, Pediococcus, and several yeasts.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Chilton SN, Burton JP, Reid G. Inclusion of fermented foods in food guides around the world. Nutrients 2015;7:390-404.
Ross RP, Morgan S, Hill C. Preservation and fermentation: Past, present and future. Int J Food Microbiol 2002;79:3-16.
Kabak B, Dobson AD. An introduction to the traditional fermented foods and beverages of Turkey. Crit Rev Food Sci Nutr 2011;51:248-60.
Rolle R, Satin M. Basic requirements for the transfer of fermentation technologies to developing countries. Int J Food Microbiol 2002;75:181-7.
Kok CR, Hutkins R. Yogurt and other fermented foods as sources of health-promoting bacteria. Nutr Rev 2018;76:4-15.
Rahayu ES. Lactic Acid Bacteria in Fermented Foods of Indonesian Origin. Agritech Journal
Bansal S, Singh A, Mangal M, Sharma SK. Isolation and characterization of lactic acid bacteria from fermented foods. Vegetos 2013;26:325-30.
Pamungkas W. Fermentation Technology, Alternative Solution in Efforts to Utilize Local Feed Ingredients. Aquaculture Media 2011; 6:43.
Mani A. Food Preservation by Fermentation and Fermented Food Products. Int J Acad Res Dev 2018;1:51-7.
Gaggia F, Di Gioia D, Baffoni L, Biavati B. The role of protective and probiotic cultures in food and feed and their impact in food safety. Trends Food Sci Technol 2011;22 Suppl 1:S58-66.
Nur HS. Formation of Organic Acids by Acid Bacterial Isolates Lactate on Durian (Durio zibertinus Murr
) Flesh Media. J Biosci2005;2;1-10.
Harzallah D, Belhadj H. Lactic Acid Bacteria as Probiotics: Characteristics, Selection Criteria and Role in Immunomodulation of Human GI Muccosal Barrier. In Book : Lactic Acid Bacteria R and D for Food, Health and Livestock Purposes Chapter 8;2013. [doi: 10.5772/50732].
Wedajo B. Lactic Acid Bacteria: Benefits, Selection Criteria and Probiotic Potential in Fermented Food. J Probiotics Health 2015;3:1-9. [doi: 10.4172/2329 8901.1000129].
Pujawan N. Efforts to improve the quality of brem madiun with the addition of sodium bicarbonate. Boga Dan Gizi 2004;3:5-9.
Tamang JP, Thapa N, Bhalla TC, Savitri. Ethnic Fermented Foods and Beverages of India. In Ethnic Fermented Foods and Alcoholic Beverages of Asia; Tamang JP, Ed.; Springer: New Delhi, India, 2016;pp:17-72.
Aryanta WR. Traditional fermented foods in Indonesia. Japanese Journal of Lactic Acid Bacteria
Ardaneswari DPC, Kumalaningsih S, Santoso, I. Production System Analysis of Brem Processing unit. Case Study: The Industrial Centers of Brem in Kaliabu and Bancong Village, Madiun District. Wacana Journal
Yuliana N. Fermentation Profile of Rusip Made From Anchovies (Stolephorus sp.). Agritech Journal
Steinkraus KH. Fermentations in world food processing. Compr Rev Food Sci Food Saf 2002;1:23-32.
Yuliana N, Koesoemawardani D, Susilawaty, Kurniati Y. Lactic acid bacteria during fish fermentation (rusip). MOJ Food Process Technol
Nam YD, Chang HW, Kim KH, Roh SW, Bae JW. Metatranscriptome analysis of lactic acid bacteria during kimchi fermentation with genome-probing microarrays. Int J Food Microbiol 2009;130:140-6.
Kim M, Chun J. Bacterial community structure in kimchi, a Korean fermented vegetable food, as revealed by 16S rRNA gene analysis. Int J Food Microbiol 2005;103:91-6.
Patra JK, Das G, Paramithiotis S, Shin HS. Kimchi and other widely consumed traditional fermented foods of Korea: A review. Front Microbiol 2016;7:1493.
Jeong SH, Jung JY, Lee SH, Jin HM, Jeon CO. Microbial succession and metabolite changes during fermentation of dongchimi, traditional Korean watery kimchi. Int J Food Microbiol 2013;164:46-53.
Jang SJ, Kim YJ, Park JM, Park YS. Analysis of microflora in gochujang, Korean traditional fermented food. Food Sci Biotechnol 2011;20:1435-40.
Lopitz-Otsoa F, Rementeria A, Elguezabal N, Garaizar J. Kefir: A symbiotic yeasts-bacteria community with alleged healthy capabilities. Rev Iberoam Micol 2006;23:67-74.
Prado MR, Blandón LM, Vandenberghe LP, Rodrigues C, Castro GR, Thomaz-Soccol V, et al.
Milk kefir: Composition, microbial cultures, biological activities, and related products. Front Microbiol 2015;6:1177.
Yüksekdag ZN, Beyatli Y, Aslim B. Determination of some characteristics coccoid forms of lactic acid bacteria isolated from Turkish kefirs with natural probiotic. LWT Food Sci Technol 2004;37:663-7.
Zanirati DF, Abatemarco M Jr., Sandes SH, Nicoli JR, Nunes ÁC, Neumann E. Selection of lactic acid bacteria from Brazilian kefir grains for potential use as starter or probiotic cultures. Anaerobe 2015;32:70-6.
Yan PM, Xue WT, Tan SS, Zhang H, Chang XH. Effect of inoculating lactic acid bacteria starter cultures on the nitrite concentration of fermenting Chinese paocai. Food Control 2008;19:50-5.
Tamang JP, Tamang B, Schillinger U, Franz CM, Gores M, Holzapfel WH. Identification of predominant lactic acid bacteria isolated from traditionally fermented vegetable products of the Eastern Himalayas. Int J Food Microbiol 2005;105:347-56.
Tamang JP, Tamang B, Schillinger U, Guigas C, Holzapfel WH. Functional properties of lactic acid bacteria isolated from ethnic fermented vegetables of the Himalayas. Int J Food Microbiol 2009;135:28-33.
Saranraj P, Naidu MA, Sivasakthivelan P. Lactic acid bacteria and its antimicrobial properties: A review. Int J Pharm Biol Arch 2013;4:1124-33.
Mountney GJ, Gould WA. Practical Food Microbiology and Technology
. New York, USA: Van Nostrand Reinhold Company; 1988.
Isitua CC, Ibeh NI. Novel method of wine production from banana (musa acuminata) and pineapple (ananas comosus) wastes. Afr J Biotechnol 2010;9:7521-4.
Dirar HA. The Indigenous Fermented Foods of the Sudan: A Study in African Food and Nutrition. Wallingford: CAB International; 1993.
El-Hadi Sulieman AM, Ilayan AA, El Faki AE. Chemical and microbiological quality of Garris, Sudanese fermented camel's milk product. Int J Food Sci Technol 2006;41:321-8.
Bornstein S. The ship of the desert. The dromedary camel (Camelus dromedarius
), a domesticated animal species well adapted to extreme conditions of aridness and heat. Rangifer 1990;10:231.
El-Zubeir IE, Babiker SA. Chemical and Microbial Measurements of Fermented Camel Milk :Gariss” From Transhumance and Nomadic Herds in Sudan. Aust J Basic Appl Sci. 2008;2800-4.
Admasu MA, Cione E. Microbiological characteristics and physico-chemical parameters of fermented milk product ergo-A traditional yogurt product of Ethiopia. Food Sci Qual Manag 2016;49:42-5.
Beyan A, Ketema T, Bacha K. Antimicrobial susceptibility pattern of lactic acid bacteria isolated from ergo, a traditional Ethiopian fermented milk, Jimma, South West Ethiopia. Ethiop J Educ Sci 2011;7:9-17.
Mulaw G, Sisay Tessema T, Muleta D, Tesfaye A. In vitro
evaluation of probiotic properties of lactic acid bacteria isolated from some traditionally fermented Ethiopian food products. Int J Microbiol 2019;2019:7179514.
Savadago A, Ouattara CAT, Bassole IHN, Traore AS. Antimicrobial activities of lactic acid bacteria strains isolated from Burkina Faso fermented milk. Pak J Nutr 2004;3:174-9.
Gonfa A, Fite A, Urga K, Gashe BA. Microbiological aspects of ergo (ititu) fermentation. SINET Ethiop J Sci 1999;22:283-90.
Fioramonti J, Theodorou V, Bueno L. Probiotics: What are they? What are their effects on gut physiology? Best Pract Res Clin Gastroenterol 2003;17:711-24.
Giraffa G, Chanishvili N, Widyastuti Y. Importance of lactobacilli in food and feed biotechnology. Res Microbiol 2010;161:480-7.
Galdeano CM, Perdigón G. Role of viability of probiotic strains in their persistence in the gut and in mucosal immune stimulation. J Appl Microbiol 2004;97:673-81.
Hekmat S, Reid G. Sensory properties of probiotic yogurt is comparable to standard yogurt. Nutr Res 2006;26:163-6.
Shu G, Lei N, Wan H, Chen H, Li H. Effect of temperature and inoculum size on goat yogurt fermented by Bifidobacterium bifidum
and lactobacillus casei. Carpathian J Food Sci Technol 2015;7:28-35.
Aragon-Alegro LC, Alarcon Alegro JH, Cardarelli HR, Chiu MC, Isay Saad SM. Potentially probiotic and synbiotic chocolate mousse. LWT Food Sci Technol 2007;40:669-75.
Rodrigues D, Rocha-Santos TA, Pereira CI, Gomes AM, Malcata FX, Freitas AC. The potential effect of FOS and inulin upon probiotic bacterium performance in curdled milk matrices. LWT Food Sci Technol 2011;44:100-8.
De Roos NM, Katan MB. Effects of probiotic bacteria on diarrhea, lipid metabolism, and carcinogenesis: A review of papers published between 1988 and 1998. Am J Clin Nutr 2000;71:405-11.
Ishikawa H, Akedo I, Otani T, Suzuki T, Nakamura T, Takeyama I, et al.
Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. Int J Cancer 2005;116:762-7.