Handbook of Indigenous Fermented Foods

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title:Handbook of Indigenous Fermented Foods Food Science and Technology (Marcel Dekker, Inc.) ; 73author:Steinkraus, Keith H.publisher:CRC Pressisbn10 | asin:0824793528print isbn13:9780824793524ebook isbn13:9780585082011language:EnglishsubjectFermented foods--Handbooks, manuals, etc.publication date:1995lcc:TP371.44.H36 1995ebddc:664subject:Fermented foods--Handbooks, manuals, etc.

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Introduction to Indigenous Fermented Foods

Keith H. Steinkraus

Institute of Food Science, Cornell University, Ithaca, New York

If you know the history of men's food, you know the history of man.

Philosophy includes theory or investigation of the principles or laws that regulate the universe and underlie all knowledge and reality. Archaeology is the scientific study of the life and culture of ancient peoples. Anthropology is the study of races, physical and mental characteristics, distribution, customs, social relationships, etc. When we start to study man's foods, we become involved in all of the above. In fact, when we study fermented foods, we are studying the most intimate relationship among man, microbes, and foods. There is a never-ending struggle between man and microbes to see which will be first to consume the available food supplies.

Religion was an attempt by humans to explain the origin of the universe, the earth, and man long before there was a scientific method or the means to study these phenomena and long before there was any knowledge of the concept of, for example, microorganisms. Such knowledge was obtained as recently as 300 years ago, when Leeuwenhoek discovered tiny animacules under his primitive lenses, and only a little more than 100 years ago, when Pasteur demonstrated the role of microorganisms in fermentation and Koch showed that microbes cause disease. And it is only in the last 50 years that the role played by polymeric deoxyribonucleic acid (DNA) in all forms of life was discovered.

According to present scientific thought, the earth is about 4.5 billion years old. The first forms of life to appear or evolve on earth were microorganisms. Fossil organisms have been found in rocks 3.3 to 3.5 billion years old (Schopf and Packer, 1987). Since then, microorganisms have had the principal task of recycling organic matter in the environment. As such they are absolutely essential to the health of the earth, whereas humans are nonessential polluters who may eventually make the earth uninhabitable.

Whether by chance or by design, it was extraordinarily fortunate that the earth was originally colonized by microorganisms that are capable of recycling organic matter. Without them, the earth would be a gigantic, permanent waste dump.

Plants were the next forms of life to evolve, according to present scientific thought, and they serve as a basis for man's food. For at least a billion years before man arrived, plants were producing food consisting of leaves, stems, seeds, nuts, berries, fruits, tubers, etc. So when humans were created or evolved on earth, the basis for their food was already present and productive.

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develop a meatlike texture. This is expensive processing and RHM/ICI have spent more than $100,000,000 developing the process and products (Yanchinski, 1984).

Indigenous Meat Substitutes

The processes described above are modern applied microbiology and sophisticated food science and technology. It is interesting that the Western world, which produces and consumes vast quantities of animal meats, has developed the advanced processes for manufacturing vegetable-protein meat substitutes. However, centuries ago, the Indonesians, without modern chemistry and microbiology, developed a fermentation product in which soybeans are soaked, dehulled, partially cooked, and inoculated with molds belonging to genus Rhizopus. Incubated in a warm place (30 to 37C), the soybeans are knitted into a compact cake by the fibrous mold mycelium in 1 to 3 days. The cake, which is over 40% protein on a dry solids basis, is sliced thin and deep fried or used as a meat substitute in soups. This product, which is called tempe kedele, has a texture that appeals to the consumer; its protein content and nutritive value make it a good substitute for meat in the diet.

Tempe can be manufactured in any part of the world where soybeans are available. The technology is simple and it is low in cost compared with spun fiber, extruded meat analogues, or even the British mold mycelium process.

An advantage of meat analogues is that everything is edible, in contrast to meats, which contain bone and other inedible components. This characteristic is also true of tempe. Everything is eaten; there is no waste.

It also should be noted that tempe is one of the first quick-cooking foods, a characteristic highly prized in Western food technology. Soybeans require 5 to 6 h boiling to soften them for consumption. After the tempe fermentation, they require only 3 or 4 min deep frying or 10 min boiling to prepare them for eating (van Veen and Steinkraus, 1970).

The Indonesians also have demonstrated how to use the tempe process to convert what are essentially animal foodstuffs to human-quality food. Oncom (Ontjom) is a food made by fermenting peanut presscake with either the tempe mold or Neurospora intermedia. Bongkrek is coconut presscake fermented with the tempe mold. In the Western world, these presscakes have been used primarily for animal feeds. Their fiber content and relative undigestibility make them less desirable for human food. However, when enzymes from the mold, which overgrows the presscakes, penetrate the substrate, the proteins, lipids, and other solids become more soluble and more digestible (van Veen et al., 1968); at the same time, flavor is improved. The end result is a food for human consumption that serves a very important role in the Indonesian diet because of its protein content and low cost. As population continues to expand, the world is going to have to review its present usage of all raw materials potentially suitable for food and convert more of its present animal feeds to human use. The tempe process is a pattern that can be applied to other waste materials.

The major fermentation product, tempe kedele, is the subject of this section and, as the reader will see, the tempe process can be used to convert a number


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Steinkraus, K. H., D. B. Hand, J. P. Van Buren, and L. R. Hackler. 1961. Pilot plant studies on tempe. In Proceedings of Conference on Soybean Products for Protein in Human Foods. USDA, pp. 7584.


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Steinkraus, K. H., J. P. Van Buren, L. R. Hackler, and D. B. Hand. 1965b. A pilot plant process for the production of dehydrated tempeh. Food Technol. 19:6368.

Stillings, B. R. and L. R. Hackler. 1965. Amino acid studies on the effect of fermentation time and heat-processing of tempeh. J. Food Sci. 30:10431048.

Sudarmadji, S. and P. Markakis. 1977. The phytate and phytase of soybean tempeh. J. Sci. Food Agric. 28:381383.

Sudarmadji, S. and P. Markakis. 1978. Lipid and other changes occurring during the fermentation and frying of tempeh. Food Chem. 3:165170.

Sudigbia, I., A. Sumantri, and D. Karyadi. 1990. The use of tempe in medical practice. In Proc. Second Asian Symposium on Non-Salted Soybean Fermentation, Feb. 1315, 1990, Jakarta, Indonesia. (Hermana, M., K. M. S. Mahmud, and D. Karyadi, eds.) Nutrition Research and Development Centre, Bogor, Indonesia.

Suparmo and P. Markakis. 1987. Tempeh prepared from germinated soybeans. J. Food Sci. 52:17361737.

Takamine, J. 1913. Making a diastatic product. U.S. Pat. No. 1,054,324.

Tanaka, N., S. K. Kovats, J. A. Guggisberg, L. M. Meske, and M. P. Doyle. 1985. Evaluation of the microbiological safety of tempeh made from unacidified soybeans. J. Food Prot. 48:438441.

Tanuwidjaja, L. 1986. Large scale tempe inoculum production. In Proc. Asian Symposium Non-Salted Soybean Fermentation, July 1517, 1985. Tsukuba Science City, Ibaraki, Japan, pp. 305309.

Tanuwidjaja, L. 1977. Utilization of defatted soybean flour in tempeh fermentation. Symposium on Indigenous Fermented Foods, Bangkok, Thailand.

Terui, G., I. Shibasaki, and T. Mochizuki. 1957. The high-heap aeration process as applied to some industrial fermentations. I. Citric acid fermentation. Hakko Kogaku Zasshi. 35:105116.

Terui, G., I. Shibasaki, and T. Mochizuki. 1958. The high-heap aeration process as applied to some industrial fermentations. II. General description of the improved process. Hakko Kogaku Zasshi. 36:109116.

Timotius, K. H. and P. Farley. 1990. Extracellular enzymes of Rhizopus oligosporus. A Review. In Proc. Asian Symposium on Non-Salted Soybean Fermentation, Feb. 1315, 1990, Jakarta, Indonesia. (Hermana, Mien KMS Mahmud, and D. Karyadi, eds.) Nutrition Research and Development Centre, Bogor, Indonesia.

Tsubaki, K. 1986. Historical survey of the studies on Mucorales in Asia. In Proc. Asian Symposium on Non-Salted Soybean fermentation, July 1517, 1985. Tsukuba Science City, Ibaraki, Japan, pp. 2830.

Tuncel, G. M., J. R. Nout, and F. M. Rombouts. 1989. Effect of acidification on the microbiological composition and performance of tempe starter. Food Microbiol. 6:3743.

Tuncel, G., M. J. R. Nout, L. Brimer, and D. Goktan. 1990. Toxicological, nutritional and microbiological evaluation of tempe fermentation with Rhizopus oligosporus of bitter and sweet apricot seeds. Int. J. Food Microbiol. 11:337344.

Underkofler, L. A., E. J. Fulmer, and L. Schoene. 1939. Saccharification of the starch grain mashes for the alcoholic fermentation industry. Use of mold amylase. Indus. Eng. Chem. 31:734738.

Underkofler, L. A., G. M. Severson, K. J. Goering, and L. M. Christensen. 1947. Commercial production and use of mold bran. Cereal Chem. 24:122.

Usmani, N. F., and R. Noorani. 1986a. Studies on soybean tempeh. Part 1. Optimization of factors effecting fermentation in commercial production of tempeh with respect to pilot plant studies. Pakistan J. Sci. Ind. Res. 29:145147.

Usmani, H. F. and R. Noorani. 1986b. Studies on soybean tempeh. Part II. Propagation and preservation of Rhizopus oligosporus spores for commercial production of tempeh from soybean. Pakistan J. Sci. Ind. Res. 29:148150.


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Van Buren, J. P., L. R. Hackler, and K. H. Steinkraus. 1972. Solubilization of soybean tempeh constituents during fermentation. Cereal Chem. 49:208211.

van Damme, P. A., A. G. Johannes, H. C. Cox, and W. Berends. 1960. On toxoflavin, the yellow poison of P. cocovenenans. Rec. Trav. Chim. 79:255267.

van Veen, A. G. 1950. Bongkrek acid, a new antibiotic. Doc. Neerl. et Indon. Morbis. Trop. 2:185188.

van Veen, A. G. 1967. The bongkrek toxins. In Biochemistry of Some Foodborne Microbial Toxins (R. I. Mateles and G. N. Wogen). M. I. T. Press, Cambridge, Massachusetts.

van Veen, A. G. and W. K. Mertens. 1933a. De bongkrek vergiftigingen in Banjumas I, Geneesk. Tijdschr. Ned.-Indie. LXXIII:12231253.

van Veen, A. G. and W. K. Mertens. 1933b. De bongkrek vergiftigingen in Banjumas II, Geneesk. Tijdschr. Ned.-Indie. LXXIII:13091342.

van Veen, A. G. and W. K. Mertens. 1934. Die giftstoffe der sogenannten bongkrek vergiftugen auf Java. Rec. Trav. Chim. 53:257266.

van Veen, A. G. and W. K. Mertens. 1935. Die Bongkreksaure, ein blutzucker-senkender stoff. Recueil des Travaux Chimiques des Pays-bas. 54:257266. 54:373380.

van Veen, A. G. and G. Schaefer. 1950. The influence of the tempeh fungus on the soya bean. Documenta Neerlandica et Indonesica de Morbis Tropicis. 11:270281.

van Veen, A. G. and J. K. Baars. 1938. The constitution of toxoflavin. Rec. Trav. Chim. 57:248253.

van Veen, A. G. and K. H. Steinkraus. 1970. Nutritive value and wholesomeness of fermented foods. J. Agric. Food Chem. 18:576578.

van Veen, A. G., D. C. W. Graham, and K. H. Steinkraus. 1968. Fermented peanut presscake. Cereal Sci. Today. 13:9699.

Wadud, S., H. Ara, and S. Kosar. 1986. Studies on the preparation of tempeh and tempeh kababs. Pakistan J. Sci. Ind. Res. 29:222226.

Wadud, S., S. Kosar, H. Ara, and H. Durrani. 1988. A process for the pilot plant production of tempeh. Pak. J. Sci. Ind. Res. 31:435438.

Wagenknecht, A. C., L. R. Mattick, L. M. Lewin, D. B. Hand, and K. H. Steinkraus. 1961. Changes in soybean lipids during tempeh fermentation. J. Food Sci. 26:373376.

Wanderstock, J. J. 1968. Food analogues. The Cornell Hotel and Restaurant Administration Quarterly, August, pp. 2933.

Wang, H. L. and C. W. Hesseltine. 1965. Studies on the extracellular proteolytic enzymes of Rhizopus oligosporus. Can. J. Microbiol. 11:727732.

Wang, H. L. and C. W. Hesseltine. 1966. Wheat tempeh. Cereal Chem. 43:563570.

Wang, H. L. and C. W. Hesseltine. 1970. Multiple forms of Rhizopus oligosporus protease. Arch. Biochem. Biophys. 140:459463.

Wang, H. L. and C. W. Hesseltine. 1979. Mold-modified foods. In Microbial Technology, 2nd edition (H. J. Peppler and D. Perlman, ed.). Academic Press, New York, vol. 2, pp. 95129.

Wang, H. L., D. I. Ruttle, and C. W. Hesseltine. 1968. Protein quality of wheat and soybeans after Rhizopus oligosporus fermentation. J. Nutr. 96:109114.

Wang, H. L., D. I. Ruttle, and C. W. Hesseltine. 1969a. Antibacterial compound from a soybean product fermented by Rhizopus oligosporus. Proc. Soc. Exper. Biol. Med. 131:579583.

Wang, H. L., D. I. Ruttle, and C. W. Hesseltine. 1969b. Milk-clotting activity of proteinase produced by Rhizopus. Can. J. Microbiol. 15:99104.

Wang, H. L., J. B. Vespa, and C. W. Hesseltine. 1974. Acid protease production by fungi used in soybean food fermentation. Appl. Microbiol. 27:906911.

Wang, H. L., E. W. Swain, and C. W. Hesseltine. 1975a. Mass production of Rhizopus oligosporus spores and their application in tempeh fermentation. J. Food Sci. 40:168170.


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of bean types and also presscakes and other by-products into nutritious, protein-rich meat analogues.

Historical Perspectives

The history of tempe as a subject has been covered by Shurtleff and Aoyagi (1984) in an 81-page book that contains 402 references.

Although tempe has been known and produced by Indonesians for centuries, it was the studies of Prinsen Geerligs (1895), who was interested in identifying the tempe mold, that ushered in the era of scientific tempe research. This was followed rather closely by Boorsma (1900) who analyzed tempe and soybeans to determine the changes that were occurring in the substrate. The next advances in the knowledge of tempe arose through the work of Jansen (1923) who showed that the thiamine content was reduced in tempe and the research of Jansen and Donath (1924) who demonstrated that tempe protein was highly nutritious when fed to animals. Tempe was described in Burkill's dictionary of Malayan plant foodstuffs (Burkill, 1935).

In the 1930s, a group of Dutch scientists working in Indonesia began an investigation of a severe poisoning that occurred occasionally in people consuming coconut residues or presscakes fermented to tempe bongkrek. In a series of classic studies, van Veen and his associates characterized bongkrek toxin into two fractionsbongkrek acid and toxoflavin (van Veen and Mertens, 1933a,b, 1934, 1935; Darwis and Grevenstuk, 1935; van Veen, 1950; van Damme et al., 1960; van Veen and Baars, 1938; Latuasan and Berends, 1961; Levenberg and Linton, 1966; van Veen, 1967; Henderson and Lardy, 1970).

Lockwood et al. (1936) made an intensive study of Rhizopus oryzae, believed to be the principal tempe mold at that time. Later, Dwidjoseputro (1961) made a similar study of Monilia sitophila, the oncom mold; and Dwidjoseputro and Wolf (1970) studied the microorganisms present in tempe inocula.

The next advances in tempe science arose during World War II when many prisoners of the Japanese had to rely upon tempe as a major protein source (Stahel, 1946; Smith and Woodruff, 1951; Grant, 1952). Soybeans were issued to the prison camps by the Japanese, but fuel was in short supply and prisoners suffering from dysentery could not digest the soybeans. However, even malnourished prisoners suffering from dysentery were able to digest and tolerate the beans in the form of tempe. Stahel (1946) was the first to report that the fungal fermentation was preceded by a bacterial acid fermentation during soaking.

Van Veen and Schaefer (1950) published their classic paper on tempe based partly upon van Veen's experiences in a prison camp. This was followed by the suggestion by Autret and van Veen (1955) that tempe be considered as a protein-rich, nutritious food for infants and children.

In 1958, Ms. Yap Bwee Hwa brought a sample of dried tempe to Cornell University and completed a research project on microbiological, biochemical, and nutritional changes occurring during the tempe fermentation (Steinkraus et al., 1960).

Mr. Ko Swan Djien arrived in Dr. C. W. Hesseltine's laboratory at the Northern Regional Laboratory about the same time, ushering in an active re-


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Wang, H. L., E. W. Swain, L. L. Wallen, and C. W. Hesseltine. 1975b. Free fatty acids identified as antitryptic factor in soybeans fermented by Rhizopus oligosporus. J. Nutr. 105:13511355.

Watkins, J. C. 1970. Applications Note ANC-19-70. Hewlett-Packard Inst. Co., Avondale, Pennsylvania.

Winarno, F. G. 1986. Tempe making on various substrates. In Proc. Asian Symposium Asian Non-Salted Soybean Fermentation, July 1517, 1985. Tsukuba Science City, Ibaraki, Japan, pp. 125141.

Winarno, F. G. and N. R. Reddy. 1986. Tempe. In Legume-based Fermented Foods (N. R. Reddy, M. D. Pierson, and D. K. Salunkhe, eds.) CRC Press, Boca Raton, pp. 95117.

Winarno, F. G., S. Hardjo, and F. Rumawas. 1976. The Present Status of Soybean in Indonesia. FATEMETA. Bogor Agricultural University, Bogor, Indonesia. 128 pp.

Worthington, R. W. and L. R. Beuchat. 1974. a-Galactosidase activity of fungi on intestinal gas-forming peanut oligosaccharides. Agric. Food Chem. 22:10631066.

Yamamoto, K. 1957a. Koji. II. Effects of some conditions of medium on the production of mold protease. Bull. Agr. Chem. Soc. Jpn. 21:313318.

Yamamoto, K. 1957b. Koji. III. Effect of cultural temperatures on the production of mold protease. Bull. Agr. Chem. Soc. Jpn. 21:319324.

Yamasaki, M., T. Yasui, and K. Arima. 1966. Pectic enzymes of microorganisms. II. Production of endo-polygalacturonase by Aspergillus saitoi. Agric. Biol. Chem. 30:142148.

Yanchinski, S. 1984. U.K. sinks its teeth into myco-protein. Biotechnology XX: p. 933.

Yeoh, Q. L. and Z. Merican. 1977. Malaysian tempeh. Symposium on Indigenous Fermented Foods, Bangkok, Thailand.

Zamora, R. G. and T. L. Veum. 1979. The nutritive value of dehulled soybeans fermented with Aspergillus oryzae or Rhizopus oligosporus as evaluated by rats. J. Nutr. 109:13331339.

Zilliken, F., & H. Chjha 1985. Novel isoflavonoides and derivatives, a powerful class of new oxidantia, radical scavengers & chelate forming substances derived from fermented soybeans (tempe). In: Abstracts Asian Symposium on Non-salted Soybean Fermentation. p. 67 Tsukuba Science City. Ibaraki, Japan. July 1517.


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2

Indigenous Fermented Foods Involving an Acid Fermentation Preserving and Enhancing Organoleptic and Nutritional Qualities of Fresh Foods

A. M. Abdel Gadir

and M. Mohamed

Department of Microbiology, Faculty of Agriculture, Food Research Centre, Shambat, Sudan

Y. Abd-el-Malek

Department of Agricultural Microbiology, Faculty of Agriculture, Cairo University, Giza, Egypt

Ibrahim Haji Ahmad

Product Research and Development, Kumpulan Fima Berhad, Tingkat 3 and 4 Blok Menara Besar, Wisma MCIS, Jalan

Barat, Petaling Jaya, Selangor, Malaysia

I. A. Akinrele

Centre for the Development of Industry, Brussels, Belgium

P. T. Arroyo,

L. A. Ludovico,

Y. N. Chiu,

H. T. Solidum,

T. Manalo,

C. N. Bigueras,

M. Lero,

and E. E. Alcantara

Department of Fisheries Technology, College of Fisheries, University of the Philippines, Diliman, Quezon City, Philippines

M. S. M. Azmey

Department of Agriculture, Hambanota, Sri Lanka

E. O. I. Banigo

Department of Food Technology, University of Ibadan, Ibadan, Nigeria

Abraham Besrat

Science and Technology Campus, Biochemistry, Addis Ababa University, Addis Ababa, Ethiopia

Chi-Hyun Chang

Pulmunone Kimchi Museum, Seoul, Korea

Roger E. Cullen

Department of Food Science and Technology, Cornell University, Geneva, New York

M. Demerdash

Baker's Yeast Factory, Alexandria, Egypt

Phrosso Economidou

Cyprus Organization for Standards and Control of Quality, Ministry of Commerce and Industry, Nicosia, Cyprus

T. D. Ekmon

Department of Quality Control and Research, Distilleries Company of Sri Lanka, Ltd., Seeduwa, Sri Lanka

R. W. Gatumbi

and N. Muriru

National Agricultural Laboratories, Nairobi, Kenya

Chaltu Gifawesen

Department of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia

Abeba Gobezie

Ethiopian Nutrition Institute, Addis Ababa, Ethiopia

Y. A. Hamdi

State Organization of Soil and Land Reclamation, Abou Bhraib, Bagdad, Iraq

P. Hartles,

J. Van Hooidonk,

and J. W. M. LaRiviere

International Institute for Hydraulic and Environmental Engineering, Delft, The Netherlands

O. Kandler

Institute of Botany, University of Munich, Munich, Germany

Tai-Wan Kwon

Food Resources Lab, Korea Institute of Science and Technology, Dong Dae Mun, Seoul, Korea

S. A. Z. Mahmoud,

W. A. Mashhoor,

S. M. El-Hosseiny,

S. M. Taha,

Y. Z. Ishac,

and M. N. S. El-Nakhal

Faculty of Agriculture, Ain Shams University, El Khema, Cairo, Egypt

S. K. Mbugua

Department of Food Science and Technology, University of Nairobi, Kabete, Kenya


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Zahara Merican

Food Technology Research Center, Malaysian Agricultural Research and Development Institute (MARDI), Kuala

Lumpur, Malaysia

Tae-Ick Mheen,

Ke-Ho Lee,

and Su-Rae Lee

Korean Society of Food Science and Technology, Choongmoo-ro, Joong-ku, Seoul, Korea

B. K. Mital

Department of Food Science, G. B. Pant University of Agriculture, Distt, Nainital, Pantnagar, U.P. India

Semyon Mogilevsky

Rochester, New York

Sabry R. Morcos

Food Science and Nutrition Research Department, National Research Centre, Sh. El-Tahrir, Dokki, Cairo, Egypt

Sunit Mukherjee,

D. R. Chaudhuri,

and H. Gangopadhyay

Department of Food Technology and Biochemical Engineering, Jadavpur University, Calcutta, India

Tilak Nagodawithana

Universal Foods Co., Milwaukee, Wisconsin

K. O. Nyako

Department of Biological Sciences, University of Science and Technology, Kumasi, Ghana

A. O. Ogunsua

Department of Food Science and Technology, University of Ife, Ile Ife, Nigeria

Nduka Okafor

Department of Applied Microbiology and Brewing, Nnamdi Azikiwe University, Awka, Anambra State, Nigeria

O. O. Onyekwere

Federal Institute of Industrial Research, Oshodi, Ikeja Lagos, Nigeria

Ke-In Park

Department of Food Technology, College of Industry, Kyung Hee University, Seoul, Korea

C. S. Pederson

Institute of Food Science, Cornell University, Geneva, New York

D. Purushothaman,

N. Dhanapal,

and G. Rangaswami

Tamil Nadu Agricultural University, Coimbatore, India

C. V. Ramakrishnan

Biochemistry Department, Faculty of Science, M.S. University of Baroda, Baroda, India

Priscilla C. Sanchez

Institute of Food Science and Technology, University of the Philippines at Los Baos, College, Laguna, Philippines

Abdul Cader Ahmed Shuaib

Department of Applied Biology and Food Science, Polytechnic of the South Bank, London, England

Keith H. Steinkraus

Institute of Food Science, Cornell University, Ithaca, New York

K. O. Stetter

Botanisches Institut der Universitt Mnchen, Munich, Germany

Ulf Svanberg

Department of Food Science, Chalmers University of Technology, Gteborg, Sweden

Q. Tongananta

and C. A. Orillo

Chemistry Department, University of the Philippines College, Laguna, Philippines

M. Ulloa,

T. Herrera,

and J. Taboada

Department de Botnica, Instituto de Biologa, Universidad Nacional Autnoma de Mxico (UNAM), Mexico, 9 D.F., Mexico

S. M. Vogel

International Development Research Centre, University of Alberta Campus, Edmonton, Alberta, Canada

Hsi-Hwa Wang

Laboratory of Applied Microbiology, Department of Agricultural Chemistry, National Taiwan University, Taipei, Taiwan, Republic of China

Po-Wah Wong

and H. Jackson

Department of Food Science, University of Alberta, Edmonton, Alberta, Canada

Brian J. B. Wood

Department of Bioscience and Biotechnology, University of Strathclyde, Glasgow, Scotland

D. Yanasugondha

Department of Biology, Kasetsart University, Bangkok, Thailand

Acid-Fermented Vegetables

113

Acid-Fermented Leavened Bread and Pancakes

149

Acid-Fermented Cereal Gruels

211

Acid-Fermented Seafood/Rice and Meat Mixtures

264

Acid-Fermented Milk and Milk/Cereal Foods

274

Pit Fermentations

308

Lactic Acid Fermented Foods for Feeding Infants

310

References

321


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Acid-Fermented Vegetables

Acid-fermented foods must have developed when mankind started collecting and storing food. Milk undergoes an acid fermentation naturally and readily; and as soon as man started collecting milk from animals, sour milk must have become an item in his diet. The acid protects the milk from spoilage by undesirable organisms in the environment. Similarly, but not as obviously, as soon as man started collecting fresh vegetables, he had the problem of maintaining their eating quality. At some point in time, he probably tried adding salt, or perhaps sea water, to the vegetable to extend its life. High concentrations of salt will preserve most foods, but the excess salt must be removed prior to consumption. During desalting, a vegetable would pass through stages favorable to acid fermentation.

We know that by the 3rd century B.C. the Chinese coolies working on the Great Wall were eating acid-fermented mixed vegetables (Pederson, 1979). Centuries ago, the Koreans developed kimchi made from acid-fermented Chinese cabbage, radish, and other ingredients. Similarly, in the Western world, cabbage was fermented to sauerkraut and cucumbers to pickles. In Africa, processes evolved for acid fermentation of gruels made from corn, cassava, and sorghum, and these products became staples in the diet.

While Ancient Egypt developed wheat breads leavened with yeasts, the people of India discovered methods for leavening cereal-legume batters with a bacterial acid fermentation. The Middle East discovered that sour milks combined with wheat resulted in dried soup ingredients with superior nutritional value and excellent keeping quality.

The advantages of acid food fermentations are: (1) they render foods resistant to microbial spoilage and the development of food toxins, (2) they make the foods less likely to transfer pathogenic microorganisms, (3) they generally preserve the foods between the time of harvest and consumption, and (4) they modify the flavor of the original ingredients and often improve the nutritional value. The Koreans also believe that acid fermentation eliminates fecal pathogens and parasites present on vegetables when human waste is applied to the soil as fertilizer.

Since canned or frozen foods are unavailable or too expensive for the hundreds of millions of the world's economically deprived and hungry, acid fermentation combined with salting remains one of the most practical methods of preserving and often enhancing the organoleptic and nutritional quality of fresh vegetables, cereal gruels, and milk-cereal mixtures. Even meats and marine products can be preserved by acid fermentation when they are combined with vegetables, cereals, or milk substrates containing fermentable carbohydrates.

Over recent years there have been a number of excellent references dealing with acid and other fermented foods (Dirar, 1993); Lorri, 1993; Steinkraus, 1982, 1983a, 1983b, 1983c, 1986, 1989; Hesseltine and Wang, 1986; Cooke et al., 1987; Chassy, 1986; Reddy et al., 1986; Westby and Reilly, 1991; International Foundation for Science, 1985, 1991; Central Food Technological Research Institute (Mysore, India), 1986; National Research Council, 1992; Yanagida et al., 1986; Aida, 1985; Wood, 1985a, 1985b; Wongkhalaung and Boonyaratanakornkit, 1986; Symposium Lactic Acid Bacteria in Foods, 1983; Second Symposium on Lactic Acid


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Bacteria, 1987; Symposium (Mexico City) on Lactic Acid Bacteria in Foods, 1985). Important developments are included in this revision but the sheer volume of the references means that readers should refer to the originals for greater detail.

Summary of Lactic Acid Fermentation Symposia (1983; 1985; 1987)

Lactic acid bacteria have been receiving ever-increasing attention because of their key roles in many fermentations. The Netherlands Society for Microbiology sponsored a Symposium on Lactic Acid Bacteria in Foods, September 79, 1983, in Wageningen. The Symposium summarized current knowledge of lactic acid fermentations in a number of areas: carbohydrate metabolism (Kandler, 1983); proteolytic systems in lactic acid bacteria (Law and Kolstad, 1983); energy transduction and solute transport (Konings and Otto, 1983); functional properties of plasmids in lactic streptococci (McKay, 1983); genetic transfer systems (Gasson, 1983); bacteriophages of lactic acid bacteria (Teuber and Lembke, 1983); mesophilic cultures in the dairy industry (Daly, 1983); thermophilic lactic cultures (Auclair and Accolas, 1983); lactic acid bacteria in meat (Egan, 1983); lactic acid bacteria in production of foods (Steinkraus, 1983b), and malo-lactic fermentation in wines (LaFon-Lafourcade et al., 1983).

The second symposium on lactic acid bacteria (1987) dealt with genetics, metabolism, and application. Papers of particular interest include those by Marshall (1987); Gurr (1987); Fernandes et al. (1987); Daeschel et al. (1987); Cooke et al. (1987); Schleifer (1987); Sandine (1987); Thompson (1987); Kashket (1987); Thomas and Pritchard (1987); Condon (1987); and Chassy (1987). The Mexican Symposium report (UNIDO. ID/WG.431/15. 1985) quotes a statement by Steinkraus (1982) in UNIDO REPORT (UNIDO/IS.336-1982):

Those involved in research on indigenous fermented foods recognize that we have only investigated the surface of a gold-mine of knowledge available on other indigenous fermented foods used daily in many relatively remote areas of the world. To complete our scientific knowledge requires that we bring all these fermentations to light, determine their essential microorganisms involved, study the biochemical changes that occur in the proteins, lipids, vitamins and other components in the substrates, determine the flavors and textures produced and how they can be controlled, and finally give the world a broader view of how microorganisms can be grown on edible substrates and contribute more to the total proteins and nutrients available for man in the future.

Important questions raised in the Mexican Symposium were: how can lactic acid cultures be mass produced, preserved, and distributed? In tropical areas will the cultures be made available as liquids, frozen, lyophilized, spray-dried, or other forms? How will the stability and activity be maintained during distribution? Can dry cultures, such as those used in making bread, be developed to overcome the distribution problem of liquid or frozen cultures? These key questions have not as yet been answered and they remain pivotal to extending many indigenous fermentations. Research is needed.

The Mexican Symposium called attention to the reports on strains of lactic acid bacteria that excrete proteins and produce amylases. Such strains would be


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of great value in many fermentations where the stability of the lactic acid/low pH would be present but starchy substrates could be hydrolyzed and protein content could be increased.

Other important questions raised in the Mexican Symposium included: Can lactic acid bacteria with unusual ability to produce organic acids, essential amino acids, such as lysine or methionine, vitamins, such as thiamine, riboflavin, or B12, or antagonistic compounds against spoilage and pathogenic organisms be isolated and then used in producing indigenous fermented foods? Can lactic acid bacteria-producing enzymes such as proteinases, lipases, pectinases, or others be found and explored? Can the amylase-producing strains or lactic acid bacteria be used to improve indigenous fermented foods based upon starch as a carbohydrate source? Can these strains be used to produce SCP from starchy foods? Can the protein content of fermented foods, such as gari, be increased by using amylase-producing lactic acid bacteria? Can genetic engineering principles be applied to these amylase-producing strains to improve the organisms? These questions posed in 1983/84 are still key to the future.

The Mexican Symposium refers to fermented foods, such as pozol, in which not only lactic acid bacteria but at least one nitrogen-fixing bacterium is involved that raises the nitrogen/protein content of the resulting fermented maize food. As yet, the ecology of the pozol fermentation and the relationship between the lactic and the nitrogen fixation have not been completely characterized. The following questions are raised: How do lactic acid bacteria affect the ability of the nitrogen-fixing organism to fix nitrogen? Can the responsible microorganisms be isolated in pure culture and combined to form a nitrogen-fixing starter culture that could be used to increase the nitrogen content of those indigenous fermented foods naturally low in nitrogen? Could the genes responsible for nitrogen fixation be transferred to lactic acid bacteria species to develop a new culture that could be used in food fermentation processes? These important questions remain to be answered.

Historical Perspectives of the Sauerkraut Literature (Carl S. Pederson)

Literature dealing with the various indigenous acid-fermented foods will be referred to under each specific food. It is necessary in the interest of enhancing the understanding of these indigenous food processes to describe the essential findings that have accumulated over the years through investigation of the typical Western acid-fermented foods-sauerkraut and pickles. It should be remembered that sauerkraut was originally an indigenous home or cottage industry. Sauerkraut fermentation is very closely related to the Korean kimchi and Chinese vegetable fermentation; and although there are some distinct differences between the sauerkraut/pickle and kimchi fermentations, knowledge of Western technology helps in understanding of the Oriental fermentations.

The extensive literature of the sauerkraut fermentation has been reviewed by Pederson and Albury (1969), and recent advances have been discussed by Stamer (1975).

Prior to 1930, Orla-Jensen (1919) had isolated strains of Betacoccus arabinosaceus, a synonym of Leuconostoc mesenteroides, from sour potatoes, sour cabbage,


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and sour dough. Orla-Jensen, however, was interested in the species only and did not associate the isolates with a role in fermentation.

In a classic study, by taking samples of fermenting sauerkraut at 2-h intervals, enumerating and identifying the microorganisms, Pederson (1930a) clearly demonstrated that a sequence of microorganisms was essential for sauerkraut fermentation. He found that the earliest stages of sauerkraut fermentation are dominated by L. mesenteroides (Tsenkovskii) (Van Tieghem, 1878) and completed by Lactobacillus brevis and Lactobacillus plantarum. At abnormally high temperatures or salt concentrations, two other species, Streptococcus faecalis and Pediococcus cerevisiae, also are involved. Gram-negative bacteria, which are very numerous on fresh cabbage, have little effect on the fermentation under normal conditions.

The fermentation of sauerkraut by a sequence of flora (Pederson, 1930a, 1930b) has been confirmed by Holtman (1939, 1941), Murray (1940), and Stamer et al. (1971). Cruess (1939, 1950) and Hohl and Cruess (1942) observed a similar sequence with lettuce; similar sequences have been observed in pickles (Costilow et al., 1956; Pederson and Ward, 1949; Pederson and Albury, 1950, 1953, 1954).

Since 1930, L. mesenteroides has been found to be important in initiating the fermentation of many vegetables, i.e., beets, turnips, chard, and cauliflower (Pederson, unpubl.); green beans and sliced green tomatoes (Pederson and Albury, unpubl.); whole head cabbage, called kiseo kupus (Yugoslavia) (Pederson et al., 1962); Brussel sprouts (Vorbeck et al., 1963); mixed vegetables (Orillo et al., 1969); Korean kimchi, (Kim and Whang, 1959); cucumbers (Pederson and Ward, 1949; Pederson and Albury, 1950; Costilow et al., 1956); olives (Vaughn, 1954, 1975); sugarbeet silage (Olsen, 1951); lettuce (Hohl and Cruess, 1942); and mostasa (Palo and Lapuz, 1955). In the latter case, there is little doubt that the isolates were strains of L. mesenteroides rather than streptococci. It is also likely that the coccoid bacteria observed microscopically by Fabian and Wickerham (1935) in fermenting dill pickles were strains of L. mesenteroides. The species has been associated with the fermentation of coffee cherries (Pederson and Breed, 1946; Frank et al., 1965).

Pederson and Albury (1955, unpubl.) studied the early fermentation of pumpernickel breads and learned that the original leavening was due to species of Leuconostoc. It is interesting to note that steamed breads such as idli of India and puto of the Philippines, both made with rice, are fermented by Leuconostoc (Mukherjee et al., 1965; Tongananta and Orillo, 1971). In many of these fermentations, the later stages are dominated by species of the genera Lactobacillus and Pediococcus. The high acidity produced by such species may tend to reduce the volume of dough.

Somewhat surprising was the observation that the fish and rice preparation, burong dalag, was also fermented in early stages by L. mesenteroides (Orillo and Pederson, 1968). Sison and Pederson (1974) also observed growth of Leuconostoc in Philippine smoked sausage.

Mold-fermented foods so commonly used in the Orient, may present some interesting aspects. Stahel (1946) noted that, during the soaking of soybeans prior to cooking and inoculation with mold for fermentation to produce tempe, the beans became acid. On the basis of our knowledge of the growth of Leuconostoc, it will not be surprising if future study shows that Leuconostoc initiates acid fermentation in the soaking of soybeans in the tempe fermentation.


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L. mesenteroides will not grow in milk; however, a closely related species, Leuconostoc citrovorum is involved in desirable milk fermentations (Hucker and Pederson, 1930).

L. mesenteroides initiates growth in vegetables more rapidly over a wide range of temperatures and salt concentrations than any other lactic acid bacterium (Pederson and Albury, 1969). It produces carbon dioxide and acids, which quickly lower the pH, thereby inhibiting the development of undesirable microorganisms and the activity of their enzymes; this may soften vegetables. The carbon dioxide produced replaces air and provides an anaerobic condition favorable to stabilization of the ascorbic acid and the natural color of the vegetable. The growth of this species modifies the environment, making it favorable for the growth of other lactic acid bacteria in the bacterial sequence.

While the importance of L. mesenteroides has been stressed, this should not imply that the roles of other lactic acid-producing species in the sequence, i.e., L. brevis, P. cerevisiae, and L. plantarum are unimportant. L. plantarum produces high acidity in all vegetable fermentations and plays the major role.

L. mesenteroides (Tsenkovskii) (Van Tieghem, 1878) cells are spherical or coccoid bacteria 0.9 to 1.2 mm in diameter, that occasionally elongate and can be isolated from the cut or bruised surfaces of many vegetable substances. They are fastidious in their growth requirements for certain amino acids, vitamins, minerals, and sugars. They will ferment glucose to about 45% levorotatory (D)-lactic acid, 25% carbon dioxide, and 25% acetic acid and ethyl alcohol. Fructose is partially reduced to mannitol and is more readily fermented than glucose. The pentoses, arabinose and xylose, are fermented to yield equi-molecular quantities of lactic and acetic acids. The combination of acids and alcohol are conducive to the formation of esters that impart desirable flavors.

L. mesenteroides will grow well and produce dextrans on sucrose media. The rubbery-to-slimy mucoid growth is so characteristic that, along with the production of lactic and acetic acid from arabinose, it can be used for species identification. The mannitol and dextrans are beneficial intermediary products in the complete fermentation; they do not contain reactive free aldehydes or ketone groups, which combine with proteins and darken foods.

L. brevis (Orla-Jensen, 1919; Bergey et al., 1934) rods are generally short and straight, 0.7 to 1.0 by 2.0 to 4.0 mm in size with rounded ends, and occur singly and in short chains. Gram or Methylene Blue stains may reveal bipolar or other granulations (Buchanan and Gibbons, 1975). L. brevis is heterofermentative, producing DL-lactic acid and gas from glucose and fructose. Optimum growth temperature is about 30C with growth occurring at 15C, but not at 45C.

L. plantarum (Orla-Jensen, 1919; Bergey et al., 1923) is a homofermentative rod, 0.7 to 1.0 by 3.0 to 8.0 mm in size, that often grows in chains or filaments and is the highest acid-producing species of this group yielding three to four times as much DL-lactic acid as the leuconostocs.

P. cerevisiae (Balcke, 1884) cells are spherical or coccoid and often occur in tetrads or groups of four. They ferment sugars to the inactive (DL) form of lactic acid. Upwards of 95% of the sugar fermented may be recovered as lactic acid and will produce about twice as much titratable acid as the leuconostocs.

All these species are gram-positive, nonsporulating, non-nitrate reducing, and nongelatin liquifying. They are microaerophilic and seldom grow on the


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surface of media. Although they require certain amino acids, they produce little change in the proteins.

The reader is referred to Kandler (1983) for a review of the carbohydrate metabolism of the lactic acid bacteria, to Kandler (1984) for a review of the taxonomy of lactic acid bacteria, and to Kandler et al. (1986) for a review of the microbial interactions in sauerkraut fermentation.

General Description of Sauerkraut

Sauerkraut or sauerkohl are German terms for sour cabbage, which is generally prepared from shredded white cabbage. The yellow-white shreds are approximately 2 to 5 mm in width and as long as 20 cm. The main countries where sauerkraut is produced are the United States and Canada in North America, and Germany, Holland, France, and other countries of Europe. Originally, sauerkraut was a home industry, but now 90% of sauerkraut is packaged commercially in cans or glass jars and more recently in flexible plastic pouches. Sauerkraut juice is also sold in some places. Sauerkraut is consumed raw or cooked with meat or sausages. In winter it is used in place of fresh vegetables. Consumption in Germany is estimated to be about 2 kg per person per year, while consumption in the United States is probably abo

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Handbook of Indigenous Fermented Foods

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