Fermented Fish Foods

Traditional Fermented Fish Products

Fermented foods currently comprise approximately one-third of the human diet globally. In traditional diets, cereal grains, dairy products, fruits, vegetables, meats, seafood and fish are all fermented using various methods as a way to preserve food and to improve its nutritional quality.

Fermentation of fish is an ancient practice. It has historically and continues to be employed to preserve fish when other methods of preservation have failed. This method of extending the harvest was born of necessity as a way of coping with seasonal scarcity. Other methods to slow bacterial degradation such as drying, salting, smoking and curing require certain ambient air temperatures and levels of humidity to be successful. Under conditions that were either too wet for drying, or when these other methods were just not feasible, fish fermentation was developed as a needed solution.

Fermentation became especially important for species of fatty fish, such as salmon, trout, Arctic char, and herring, which are not very suitable for drying due to the presence of large amounts of polyunsaturated fatty acids. In addition, fermentation developed as a way to preserve fish using less salt, as salt was expensive and generally scarce in ancient times.

The processes used in fish fermentation vary greatly worldwide, and depend on the culture, climate, and availability of both salt and fish. The species of fish and or shellfish that are fermented have always been determined by what is abundant in a given locale.

The acceptance of the aromas and taste of fermented fish sauces, pastes, and other fish food products is culturally specific. What tastes good is in part determined by familiarity and cultural upbringing as well as genetically determined taste preferences and aversions. Fermented fish products have been variously described as tasting “meaty,” “fishy,” “cheesy,” and “ammonialike.” The combination of the assorted chemical products of fermentation determines which flavors predominate.

Of all fermented foods, fermented meats and fish are the least stable, and present several challenges, such as the risk of contamination with pathogenic bacteria, namely Clostridium botulinum, and the formation of potentially toxic biogenic amines in the food product. These concerns are much more prevalent in fermented meat and fish than in other categories of fermented foods.

As fermentation expert Sandor Katz remarks in his book, The Art of Fermentation: “Fermented fish can definitely force us to confront and perhaps challenge the slippery and elusive boundary between what is and is not fit to eat.”

Currently there is a resurgence of interest and a revival in traditionally fermented foods such as sauerkraut, yogurt, sourdough bread, kombucha and the like. Fermented fish products, while new to many, have a long history as health-giving, nutritious foods that impart unique flavors, aromas, textures, and nutrients to the diet. An overview of some of the more notable fermented fish products from around the world, as well as information regarding safety and health benefits, are reviewed here.

FISH SAUCE

Fish sauce has been called “the mother of all condiments.” Garos and garum, the first known historical fish sauces, were prepared by fermenting fish blood and intestines in a salt brine. The proteolytic (protein-digesting) and lipolytic (fat-digesting) enzymes naturally present in the fish guts along with fermentative lactic acid bacteria (LAB) cause these mixtures to undergo “autolysis” or “self-digestion,” resulting in a liquid fish ferment. Garum was widely used in the ancient Greco-Roman world over two thousand years ago, particularly in ancient Rome, where it was invented to preserve fish and prevent normal decomposition. As a condiment, it was thought to be an important contributor of salt to the Roman diet. Samples of garum from preserved containers in Pompeii have been analyzed and the contents were comparable to modern fish sauces produced in both Italy and Southeastern Asia (Smirga et al.).

Fall2015-birks-pic1
Asian Fish Sauce

The original catsup or ketchup is our inherited legacy from the historical garum. “Ketchup” is an Anglicization of a Chinese dialect word which literally means “brine of pickled fish.” Early British ketchup recipes contained anchovies, shallots, wine, vinegar, spices and peppers (Smith). There once were hundreds of ketchup formulations, many of which were similar to modern fish sauces. Unfortunately, the industrialized food product we know as ketchup today is a corn-syrup sweetened concoction of vinegar and tomatoes which bears no resemblance at all to the original pickled fish liquid. In comparison, Worcestershire sauce may more closely approximate ancient garum, as it is still made with fermented anchovies.

Fish sauce is perhaps the most widely used and accepted form of fermented fish. In Southeast Asia fermented fish sauce is the fourth most important commodity. In Southeast Asian cuisines it is used to impart unique flavors and to provide an inexpensive source of protein in the form of free amino acids and peptides. As a source of bioavailable protein fish sauce has improved the nutritional profile of a diet based mainly on polished rice. Analysis of nam-pla or nam–phrik (Thai fish sauce) found that the amount of soluble protein was 50-60 percent in the form of free amino acids. Fish sauce provides the savory taste or umami, which increases overall enjoyment of a meal thanks to the presence of free amino acids that stimulate taste receptors, such as free glycine, alanine and glutamate.

Nam-pla is produced by fermentation of salted Sardinella species of fish. The whole fish is mixed with salt in a 3:1 or 3:2 ratio of fish to salt and left to ferment for twenty-four to forty-eight hours. It is later transferred to holding tanks that maintain a temperature of 35-40 degrees C for six to twelve months. The liquid is then decanted and filtered to produce the final sauce product.

Each Southeast Asian culture produces its own unique version of fish sauce, similar to nam-pla. Laos, Korea, Cambodia, Vietnam, the Philippines, as well as China and Japan each have traditional methods of preparing fish in this manner. The recipes and methods used vary from one region to another. Some use raw fish, some dried fish; some come from only a single species of fish, others use a mixture of species including shellfish; some use the whole fish, while others are prepared with only the fish viscera. A source of carbohydrate such as sugar may be added to enhance LAB fermentation, and a wide variety of herbs and spices may be added for flavor, as well as to slow down the growth of pathogenic bacteria.

FISH PASTE

Like fish sauce, fish paste is a traditional condiment in Southeast Asia, prepared by salting and fermenting fish or shellfish. Here, fish is fermented until it reaches the consistency of a soft paste or purée. Classic examples are prahok, fish paste from Cambodia prepared from crushed, salted and fermented mud fish, and kapi or Cambodian shrimp paste. In Korea, salted and fermented fish products including pastes are known as jeotkal (also jeotgal or jeot). Fish paste may also be prepared by grinding cooked fish into a soft paste, although this form of fish paste does not confer any of the health benefits of a true fermented food. Highly flavorful and salty, fish pastes are added to soups, rice and other foods. Fish pastes are often prepared from “by catch” or fish refuse that would otherwise go to waste. In this way, fish paste may be seen as a sustainable means of adding protein and other nutrients to the diet.

BRINED AND FERMENTED FISH

Pickled herring, a traditional brined food, does not involve significant fermentation, but uses salt and the enzymatic activity of proteolytic enzymes contained in the pyloric caecum of the herring to aid preservation. The pyloric caecum portion of the fish viscera is left in place when the fish are gutted. Here, enzymes break down the fish proteins in the herring and transform both its texture and taste. The herring is later washed to remove some of the salt, then pickled in a spiced vinegar. Although not a completely fermented product, it is a common delicacy that many people are familiar with. Pickled herring is mild in flavor and texture compared with some of the fully fermented fish products. It is also an excellent source of omega-3 fatty acids. Being low on the food chain, small fish such as herring and anchovies are less contaminated with heavy metals such as mercury and cadmium, so may be a better choice than some of the larger cold water fish.

Surstromming is a traditionally fermented Swedish herring prepared by submerging the pre-salted, gutted fish (pyloric caecum intact) in a 17-percent brine solution and left to ferment in barrels at 15-18 degrees C for a month. Surstromming relies on both enzymatic and fermentative processes in its preparation.

Rakfisk (“rakr”= wet, “fisk” = fish) is Norwegian fermented trout. Its preparation involves a process similar to that of surstromming. Here, salted (4-6 percent salt) gutted trout or Arctic char are layered under pressure in tight containers and stored at low temperatures (3-7 degrees C) for three to twelve months. The production of rakfisk involves both proteolytic enzyme degradation from the fish enzymes and bacterial fermentation by LAB, specifically Lactobacillus sakei. Rakfisk is regarded as a Norwegian specialty food, eaten from late fall until the Christmas season. This tradition stems from the fishing of trout or char in late summer, the prepared fermented fish being ready to eat by late fall (Skara et.al).

FERMENTED FISH AND RICE

Many cultures prepare fermented fish in combination with a grain, such as rice or millet. Nare zushi is the Japanese traditional method of preparing meat, poultry or fish with rice through an extensive, two-part, year-long process of fermentation. Modern sushi derives from a form of nare zushi called haya zushi or “quick zushi.” In making haya zushi, the complex, two-step process of fish and rice fermentation by LAB is replaced by simply mixing the rice with rice vinegar. Rice vinegar provides the tart, acidic taste traditionally imparted through lactic acid fermentation by LAB, but does not confer any of the benefits of fermentation.

Burong is a Filipino style of fish fermented with rice, where the fermented mixture of fish and rice are cooked before consuming.

Balao-balao is Filipino fermented shrimp prepared by mixing cleaned, salted shrimp with cooked rice. Both rice and shrimp are packed into covered glass jars and allowed to ferment at tropical room temperatures.

There are many other fermented fish products consumed as condiments and protein-rich additions to the diet worldwide. Wherever coastal people live, there will be found some form of fermented fish, which may include crustaceans, mollusks or cartilaginous fish in addition to bony fin fish. Inland, fermented freshwater fish products from lakes, streams and rivers are also widely used, although to a lesser degree than in coastal communities.

BENEFICIAL MICROORGANISMS

The most obvious benefits of fermented fish products are the lactic-acid-producing bacteria (LAB) and other beneficial microbes of fermentation. Research on the microbiota of the human gut supports the importance of eating fermented foods for maintaining overall health. Friendly flora in the gut support a healthy immune system, digestive and mental health, enhance detoxification, may influence weight and body composition, and much more. Studies on the human microbiome suggest that modern birth and child feeding practices, such as birth in a hospital setting, a high rate of C-sections, and a lack of extended breastfeeding may be risk factors which contribute to a substantial loss of biodiversity of these crucial health-promoting microorganisms. Eating a wide variety of fermented foods may be one strategy to ameliorate the effects of this loss.

Fall2015-birks-pic2
Traditional pickled herring with sour cream, potatoes and hard boiled egg.

ENHANCED NUTRITIONAL CONTENT

Fermentation of protein-rich food (such as fish) enhances the overall protein content and bioavailability of the protein in the food. Multiple feeding studies in animals support traditional wisdom that fermented foods provide a more bioavailable and digestible form of protein. LAB present in fermented foods have been shown in numerous studies to produce vitamins, including several B vitamins and vitamin K2. Which vitamins are produced is to a large extent dependent on the specific cultures that are present in the ferment.

TOXIC REDUCTION

In general, the process of fermentation has been shown to reduce toxic components in food. In one dramatic example, a recent study showed that the deadly nerve toxin in fugu or puffer fish (terodotoxin) was virtually eliminated by traditional methods of food preparation such as prolonged fermentation, and that it yielded a non-toxic, edible food product (Anraku et al.). It is well established that some anti-nutrients in plant foods are degraded during fermentation and it stands to reason that fermentation of fish products may result in fewer naturally present toxins as well.

BIOACTIVE MARINE PEPTIDES

Bioactive marine peptides are released from fish proteins during fermentation. These include a number of unique marine compounds with health benefits. Some bioactive marine peptides are sold as nutraceuticals, for example SeaCure, a fermented cod protein concentrate marketed for digestive health, and Katsuobushi peptide, an ACE inhibitor made from dried bonito fish. Several other ACE inhibitor peptides have been isolated from fermented fish sauce as well, showing the potential value of fish sauce as part of a diet to maintain healthy blood pressure (Ichimura et al.). Other marine bioactives have gained FDA approval as drugs, such as Ziconotide, a potent analgesic from the marine cone snail, and Adcetris, an FDA-approved cancer treatment for classical Hodgkin’s lymphoma derived from the sea hare, a type of sea slug. Traditionally fermented fish products such as fish sauce and fish paste may confer health benefits that have yet to be discovered.

BACTERIOCINS

Bacteriocins are anti-microbial isolates produced by salt-tolerant or halophilic species of LAB, such as those used in fermentation of fish products. These food components are currently being researched as alternative methods of food preservation. Budu, a fermented anchovy sauce of southern Thailand and Malaysia, was found to contain bacteriocins active against both gram negative and gram positive bacteria (Liasi et al.). Jeot-gal a salted, fermented Korean fish product contains lacticin NK24 (Lee et al.) while plaasom, a Thai fish sauce, was found to contain Weissellicin 110, active against gram positive bacteria. Nisin, a naturally derived bacteriocin from Lactococcus lactis bacteria in fermented dairy is already widely used as an approved food preservative (Cleveland et al.).

SAFETY CONCERNS: BIOGENIC AMINES

LAB are non-toxic, non-pathogenic bacteria. Select strains of LAB can produce biogenic amines (BA) through the decarboxylation of amino acids. Biogenic amines include tyramine, histamine, tryptamine, spermidine, spermine as well as putrescine and cadaverine. In bacteria, BA are defenses against an acidic environment. They are thought to enhance bacterial survival under acidic stress and may also have other important physiological roles to play, such as protection against oxidative stress and protection of bacterial DNA.

Biogenic amines are normally degraded in the human body by the monoamine oxidase (MAO) enzyme system. Biogenic amines are more problematic in certain individuals, such as those with impaired genetic detoxification ability, users of certain medications and migraine headache sufferers. If BA are not metabolized completely and enter into systemic circulation, they cause an increase in catecholamines, activating the stress hormone system. Symptoms may include flushing, increased heart rate, increased blood pressure, and migraine headache. The MAOI (monoamine oxidase inhibitor) diet restricts biogenic amines, including those from fermented foods.

Additionally, biogenic amines such as both putrescine and cadaverine can react with nitrite to form carcinogenic nitrosamines. For these reasons, commercial fermented fish products have clear limits on the acceptable amount of biogenic amines such as histamines, although the acceptable upper limits vary among countries.

Biogenic amines are considered contaminants in the food supply and can accumulate at toxic amounts. Detection of the presence of bacteria possessing the decarboxylase enzyme activity is important in food manufacturing. According to FDA guidelines, 5 mg per 1000 g is the allowable limit on histamines in food. Today, the use of starter cultures that are unable to produce biogenic amines or the use of biogenic amine-degrading enzymes limits the amount of BA in the food supply.

PUTREFACTION VS. FERMENTATION

Lactic-acid bacteria (LAB) fermentation of food products has existed since the beginning of civilization for the express purpose of eliminating from the food supply harmful putrefactive, anaerobic and pathogenic microorganisms. In particular, this is very important for flesh foods such as meat and fish.

Putrefaction, also known as decomposition or “rotting,” is very different from lactic acid fermentation. The formation of the biogenic amines putrescine and cadaverine are biomarkers for incomplete lactic acid fermentation. Both are foul-smelling, toxic compounds produced during putrefaction. Cadaverine is a breakdown product of the amino acid lysine, while putrescine derives from the amino acid ornithine. Both components are formed during the decomposition of the proteins in rotting meats and fish through anaerobic bacterial action. Interestingly, trace amounts of these compounds are often present in fermented meat products (such as dry cured sausages or strong cheeses) where they contribute to the overall flavor profile without causing any harm to human health.

The formation of biogenic amines is affected by many factors and the process requires tight control. A top-quality manufacturing facility can optimize environmental conditions to allow only beneficial microorganisms to thrive and for complete fermentation to occur. Numerous studies of less-than-optimal sanitary conditions or in developing countries where there is a lack of knowledge, experience or resources have demonstrated that there are numerous factors to be considered when determining the safety and edibility of fermented meat and fish products. See the sidebar on page 78 for a detailed list of safety considerations.

Truly, it is the environment that selects the bacteria! Since the safety, nutritional profile and palatability of fermented fish products are determined by the microorganisms present, and because there is a wide range of variation in the nutritional quality of fermented fish products, it makes sense that those techniques proven to have nourished generations of human beings on this planet should be considered reliable and of great value and interest to those who eat a traditional diet.


SIDEBAR

FACTORS AFFECTING BIOGENIC AMINE FORMATION AND MICROBIAL COMPOSITION IN FERMENTED FISH PRODUCTS

• MICROBIAL CULTURES PRESENT. These may be “wild type” microorganisms or added as commercial “starter cultures” or whey inoculants. Note that only certain bacterial strains can form biogenic amines.

• MOISTURE CONTENT. Submerged culture fermentation is defined as “fermentation under conditions of high moisture content.” This highly effective method is used in the preparation of fish sauces and pastes.

• pH. Acidity favors lactic acid bacteria (LAB) and discourages the formation of biogenic amines.

• SALINITY. A higher salt concentration discourages putrefaction and the formation of biogenic amines. At 10 percent salinity Clostridium botulinum is eliminated. Higher or lower amounts of salt are also used in traditional food preparation. If salt content is less than 10 percent, the use of additives such as sugar, spices, and starter cultures, as well as methods of drying, curing, and acidification are used in combination to produce a safe food product.

• SURFACE AREA. Grinding and chopping meat and fish into smaller pieces increases the rate of fermentation, as well as the development of biogenic amines. Note that the interior of a whole fish is sterile and only cut flesh and surfaces will contain bacteria.

• SANITATION OF FACILITIES. With the processing and storage of raw and finished materials, cleanliness is of utmost importance. It is especially important to avoid contact with soil, which may contain pathogenic microorganisms. Storage times can influence overall microbial content and quality.

• PRODUCTION TIME. From start to finish, microbial diversity changes in a predictable manner, based on other factors such as pH, salinity, temperature, enzymatic activity, etc.

• TEMPERATURE. Higher temperatures speed up both the processes of fermentation and decomposition, while cooler temperatures slow it down.

• ADDITIVES. Sugar, spices, and starter cultures can be added to the product to encourage the growth of beneficial LAB and discourage pathogenic bacteria formation.

• ENZYMES. Proteolytic enzymes are naturally present in fish flesh and visceral organs. These aid in the breakdown of fish proteins.


RESOURCES

The Art of Fermentation, Sandor Ellix Katz, Chelsea Green Publishing, 2012.

Importance of Lactic Acid Bacteria in Asian Fermented Foods, Rhee et al., Microbial Cell Factories 2011, 10 (Suppl 1):55.

Fermented and Ripened Fish Products in the Northern European Countries, Torstein Skara et al., Journal of Ethnic Foods, March 2015, Vol 2(1): 18-24.

Flavor of Fermented Fish Sauce, Robert C. McIver et al., Journal of Agricultural and Food Chemistry, Nov. 1982, Vol. 30, 6: 1017-1020.

Amino Acids and Minerals in Ancient Remnants of Fish Sauce (Garum) Sampled in the “Garum Shop” of Pompeii, Italy, Miro Smirga et al., Journal of Food Composition and Analysis, Aug. 2010, Vol.23 (5): 442-446.

“From Garum to Ketchup. A Spicy Tale of Two Fish Sauces,” Andrew F. Smith in Fish: Food from the Waters: Proceedings of the Oxford Symposium on Food and Cookery, Harlan Walker, ed., Prospect Books, 1998.

Acceleration of Autolysis During Fish Sauce Fermentation by Adding Acid and Reducing Salt Content, Asbjorn Gildberg, et al., Journal of the Science of Food and Agriculture, Vol. 35, Issue 12, 1363-1369, Dec. 1984.

Antimicrobial Activity and Antibiotic Sensitivity of Three Isolates of Lactic Acid Bacteria from Fermented Fish Products, Budu, Liasi, et al., Malaysian Journal of Microbiology, 5(1). pp 33-37.

Bacteriocins: Safe, Natural Antimicrobials for Food Preservation, J. Cleveland et al., Int. J Food Microbiol. 2001, Dec 4;71 (1):1-20.

Partial Characterization of Lacticin NK24, a Newly Identified Bacteriocin of Lactococcus lactis NK24 Isolated from Jeot-gal; N.K. Lee, H.D. Paik, Food Microbiology, Feb. 2001, Vol. 18(1):17-24.

Angiotens in I- Converting Enzyme Inhibitory Activity and Insulin Secretion Stimulative Activity of Fermented Fish Sauce; Toshiaki Ichimura, et al., Journal of Bioscience and Bioengineering, Dec. 2003, Vol 96(5); 496-499.

Fermented Fish Oil Suppresses T helper 1/2 Cell Responses in a Mouse Model of Atopic Dermatitis via Generation of CD4+ CD25+ Foxp3+ T Cells, Sang-Chul Han et al., BMC Immunology, 2012, 13-44.

Bioavailability of Marine n-3 Fatty Acid Formulations, J Dyerberg, et al., Prostaglandins Leukot. Essent. Fatty Acids. 2010 Sept; 83 (3): 137-41.

Removal of Toxin (tetrodotoxin) from Puffer Ovary by Traditional Fermentation, Anraku K et al., Toxins, 2013, Jan 18:5 (1): 193-202.

Histamine Contents of Salted Seafood Products in Taiwan and Isolation of Halotolerant Histamine-Forming Bacteria, Chung-Saint Lin, et al., Food Chemistry, March 15, 2012, Vol. 131 (2): 574-579.

Biogenic Amines in Fermented Foods, Spano G, et al., European Journal of Clinical Nutrition, 2010 Nov; 64 Suppl. 3:95-100.

Biogenic Amines in Commercially Produced Yulu, a Chinese Fermented Fish Sauce, Wei Jiang et al., Food Additives & Contaminants: Part B, Volume 7, Issue 1, 2014, 25-29.

Biogenic Amines in Jeotkals, Korean Salted and Fermented Fish Products, Jae-Huyung et al., Food Chemistry, Nov. 2002, Vol. 79 (2): 239-243.

The Problem of Biogenic Amines in Fermented Foods and the Use of Potential Biogenic Amine-Degrading Microorganisms as a Solution, Miguel A. Alvarez, et al., Trends in Food Science & Technology, Oct. 2014, Vol.39(2): 146-155.

Fermented Meat Products: Organoleptic and Biogenic Amines: A Review, V.P. Singh, et al., American Journal of Food Technology, 2012. pp 1-11.

Bacterial Diversity and Functionalities in Food Fermentation, Frederic Ravyts et al., Eng. Life Sci., 201, 12, No.4, 356-367.

The Role of Lactic Acid Bacteria in Safety and Flavour Development of Meat and Meat Products, Lothar Krockel, Chapter 5, Lactic Acid Bacteria, R&D for Food, Health and Livestock Purposes.

“Fermented Fish Products,” Applications of Biotechnology to Traditional Fermented Foods, 1992, p.13.

This article appeared in Wise Traditions in Food, Farming and the Healing Arts, the quarterly journal of the Weston A. Price Foundation, Fall 2015

Alison Birks earned a M.S. in human nutrition and holds five certifications in herbal medicine and related fields. She is proud to be a professional member of the American Herbalists Guild, one of the most prestigious organizations in her field. Alison is a motivating public speaker, published author, creative product developer, academic instructor, health coach, and radio, TV and print media personality. She is a lead instructor and science curriculum developer at the Institute of Sustainable Nutrition in West Granby, CT ( tiosn.com) as well as an instructor at Charter Oak State College. Alison maintains a busy private practice in Woodbury, CT and can be reached at alisonbirks.com

2 Responses to Fermented Fish Foods

  1. al dell says:

    specifically, am interested to learn the pro / con of k2 menaQ7 to take along withcalcium (algae-based) and a separate dose of d3?? any input to help me to better determine the acceptability and / or dosage amounts?

    txs, al

  2. al dell says:

    additionally, i take a product ‘optimized curcumin (longvida) … dosage one 500mg vegetable capsule per day … what are the pro / con again re: interaction w/ k2 menaQ7 + cal (algae based) + d3??
    what might be the the more safe levels to ingest daily … either together or separtely during day at different meals?
    txs for the input and suggestions. al.

Leave a reply

© 2015 The Weston A. Price Foundation for Wise Traditions in Food, Farming, and the Healing Arts.