- Tofu, a food product made from soybeans (Glycine max (L.) Merr), is a dietary staple in Chinese and Japanese cuisines.
- A high-quality source of calcium, isoflavones, and plant-based protein, tofu is produced by curdling soymilk with a calcium or magnesium salt. It can be consumed without further cooking.
- Tofu is widely available in both specialty and standard grocery stores, usually as a dense off-white gelatinous product, prepackaged in a plastic tray with the tofu immersed in water and covered by a plastic film.
- Tofu has been linked to outbreaks involving Yersinia enterocolitica, as well as Clostridium botulinum type A, and should be stored at less than 41°F and consumed before the stated expiration date on the package (and within 3-5 days once opened) to reduce the risk of foodborne illness.
- With the increasing popularity of vegetarian and vegan diets in the U.S. and the expanding global needs for sustainable food sources, tofu consumption in the U.S. is expected to rise in the coming years.
Soybeans, Glycine max (L.) Merr, are the main component of tofu and have a broad array of applications. Belonging to the Fabaceae, or pea family, soybeans provide a high-quality source of plant-based protein and measure similarly to animal proteins in amino acid content, amino acid bioavailability, and protein digestibility. Traditional foods made from soy are categorized as fermented (e.g., tempeh, soy sauce, and miso paste) or non-fermented (e.g., soymilk, soy flour, and tofu). Fermentation is a process used to preserve perishable foods and enhance their nutritional properties and involves the use of a mold or bacteria to convert organic molecules in food into alcohol or organic acids.
Tofu comes in a variety of textures, ranging from soft to extra-firm, and is characterized by its pale off-white color. The process of making tofu involves the curdling of the soy protein with a calcium or magnesium salt to produce a gelatinous product that has a relatively high water content, soft texture, and bland flavor. Due to its bland nature, it is used in a variety of dishes, from soups and salads to entrees and desserts.
The origins of tofu trace back to 965 CE in China. Although popular theories about the true origin of tofu remain contested, the consensus remains that it originated in China and was introduced to other parts of the world through immigration and globalization. In 1966, the tofu packaging method still used today was first implemented. The tofu is placed in a plastic, water-proof container, immersed in water to maintain shape and moisture, and sealed with a plastic film. Historically, soy consumption was limited to Chinese and Japanese populations across the world. However, with the rising popularity of vegan and vegetarian diets, soy consumption has increased in non-Chinese and non-Japanese populations in Western countries as well.
Foodborne outbreaks associated with tofu are rare, though during industrial production, home fermentation, and food preparation, there are opportunities for contamination. Due to its high moisture and nutrient content, tofu provides an environment conducive to microorganism growth. Some examples of opportunities for contamination of soybeans and tofu products include:
- Soybeans that come into contact with unclean agricultural water sources, wildlife feces, and contaminated soil.
- When manure from diseased livestock is used on soy crops.
- Cross-contamination occurs between workers’ hands or gloves, unclean containers, and the tofu at any stage of production.
- There is improper refrigeration during transportation of soybeans from processing plant to tofu factory.
- Unsanitary conditions and inadequate personal hygiene at tofu factories—fecal contamination can occur at this stage.
- Unclean water sources used to clean and boil soybeans and use in the final tofu product.
- Improper refrigeration of tofu during storage and display at grocery stores.
- Home-fermentation by consumers can increase the risk of foodborne botulism.
1981-1982 Washington State Outbreak of Y. enterocolitica
From December 1981 to January 1982, an outbreak of gastroenteritis caused by Yersinia enterocolitica affected 87 individuals in Washington State. In January 1982, local health departments were notified by two hospital labs of 12 positive stool cultures of Y. enterocolitica. This exceeded the county’s expected number for the entire year. Cases were defined as any person who was culture positive or who had come in contact with a case and had a fever with either diarrhea or abdominal cramping. Of the 87 total cases, 56 were culture-positive and ranged from 1-18 years old. Symptom duration ranged from one day to over two months and included wound ulcers, pneumonia, labial infection, arthritis, fever, diarrhea, bloody stools, joint pain, and skin rash.
In a case-control study comparing cases to age and neighborhood-matched controls, Y. enterocolitica infection was found to be statistically significantly associated with tofu consumption; those who ate tofu were 17 times more likely to become ill than those who did not. Of the 87 total cases included in the study, 80 (80.5%) had consumed a specific local brand of tofu within two weeks of symptom onset. In the investigation of the tofu plant that followed, the county identified unsanitary conditions attributed to improper personal hygiene and unclean equipment. A recall of the product was voluntarily placed in late January, and further investigation identified Y. enterocolitica in the tofu, in the untreated spring water supply, and within the plant itself. High fecal coliform counts within the tofu indicated fecal contamination as well. To address this, a water-purification system was installed at the plant and production continued soon after.
2006 Foodborne Botulism from Home-fermented Tofu in California
In November of 2006, an elderly Chinese couple living in Orange County, California was admitted to the intensive care unit after experiencing double vision, difficulty swallowing, slurred speech, and hypersalivation. The couple’s treating physicians assessed both patients’ symptoms and notified the Orange County Health Care Agency (OCHCA) of two suspected cases of botulism. Stool samples were collected from both patients and sent for testing. Clostridium botulinum type A, known to cause human illness, was detected in enrichment cultures of both stool samples. Upon interviewing the couple and visiting their home, the OCHCA found that both patients had recently consumed home-fermented tofu. Samples of the home-fermented tofu tested positive for C. botulinum type A and were found to have a high pH of 6.8.
C. botulinum is a spore-forming bacterium that is of particular concern with tofu because it grows in low-acidity foods (tofu has a pH of approximately 7.0), it can withstand the high temperatures involved in processing and pasteurization, and it flourishes in anaerobic conditions present in both water-packed and vacuum-packed tofu. According to the interview with the patients, the tofu fermentation process involved boiling and marinating the tofu followed by continuous storage at room temperature, all of which, along with the near neutral pH, likely facilitated the growth of C. botulinum. Ingestion of C. botulinum can lead to foodborne botulism and potentially cause paralysis or death. C. botulinum exists naturally in the environment and can be spread through water and soil, but is normally inhibited by proper food preparation and storage. Storage at less than 39.2°F by producers and consumers is essential to prevent the growth of C. botulinum and production of the associated neurotoxin and other microorganisms. This was the first reported case of botulism from home-fermented tofu in the U.S., but in China, where home fermentation of soybean products is mainstream, it is one of the most common sources of botulism infection.
In the 2018/2019 growing season, 360 million metric tons of soybeans were produced globally, wherein 120 million metric tons were produced in the U.S. Approximately one quarter of U.S. soybean production is exported, with the majority of crops being exported to China, the European Union, and the United Kingdom. Iowa and Illinois are the largest producers of soybeans in the U.S. as they together grow nearly a third of all U.S. soybeans. A majority of soybeans are processed into soybean oil, used in cooking and food products, and soybean meal, used for animal feed. In comparison, a small amount of U.S. soybeans are processed into other food products for human consumption, such as tofu, tempeh, soy sauce, and textured vegetable protein.
Tofu production involves four main steps: preparation of soybean milk, coagulation of the soybean milk, pressing the tofu, and pasteurizing and packing the tofu.
Preparation of Soybean Milk
First, the dry soybeans are thoroughly washed to eliminate spore-forming bacteria and dirt from the surface of the beans. The beans are then soaked for several hours(sometimes overnight)to ensure maximum hydration. Next, the beans are drained, rinsed, and ground with water. Soybeans are sometimes dehulled prior to grinding, which involves removing the outer shell of the soybean and serves to soften the bean flavor of the final product. Grinding can be done using micro-cutters, hammer mills, or other devices, and the extent to which the soybeans are ground determines the amount of protein extracted as well as the final product yield. The ground soybean and water mixture is heated to between 212°F and 230°F and boiled for three to ten minutes, denaturing the soy protein and further reducing the strong bean flavor. Once boiled, the mixture is filtered using a cheesecloth or centrifuge, producing a smooth and creamy soybean milk.
Coagulation of Soy Protein
Coagulation is the most crucial step in the tofu-making process and is what allows the soybean milk to thicken into a solid. The kind of coagulant used is determined by the type of tofu being produced—soft (silken) tofu varieties require different coagulants than firm tofu varieties. The two main kinds of coagulants are calcium sulfate (gypsum), which helps enhance the flavors naturally found in soybeans, and a mixture of magnesium chloride and calcium chloride (nigari salts), which is used to produce softer tofu. Other less common coagulants include edible acids and enzymes like proteases. Soymilk is coagulated by adding the coagulant gradually while stirring the milk and maintaining the mixture at a temperature between 140°F and 194°F. The end product of this step is a soybean curd.
Pressing the Tofu
This next step varies based on the kind of tofu being produced (silken, firm, etc.). Silken tofu, the smoothest kind with the highest water content, does not require any pressing and is coagulated in the final package. Firmer tofu varieties are pressed using a hydraulic press or centrifuge. Pressing serves to release excess liquid to manipulate the final texture and density. Once pressed, the tofu can be cut and packaged.
Pasteurizing and Packaging
Pasteurization is the process of heating a product to high temperatures for a set period of time in order to eliminate foodborne pathogens such as Escherichia coli and Yersinia enterocolitica, as well as to extend the shelf life of the finished product. During standard tofu production, soybeans (rather than the final tofu product) are heated to high temperatures, which helps to eliminate heat-sensitive pathogens, prior to any pasteurization process. For this reason, pasteurization is not required of tofu later in the process, and the FDA does not distinguish between pasteurized and unpasteurized tofu, yet almost all tofu in the U.S. is pasteurized. Among the pasteurization methods used in tofu processing are Radio Frequency Alternating Current and hot water immersion. Tofu is often packaged in a deep plastic tray filled with water and covered by a plastic film, all of which help to protect the product from contamination and to maintain moisture. Tofu can also be packaged aseptically using ultra-high temperature (UHT) sterilization to create a shelf-stable product that is fresh and safe from pathogenic microorganisms.
The finished tofu product has a high protein content (7g protein per 3 oz. serving size), a pH value of approximately 7.0, and a soft and bland flavor. Tofu water content varies depending on cultural norms as well as cooking needs. In China, a lower water content (50-60%) is preferred, making for a chewy and dense product. A higher water content (87%-90%) is popular in Japan, creating a very soft and fragile tofu, like what is used in miso soup. In the U.S., tofu water content generally falls in the middle (75-80%).
Multiple varieties of tofu are available to U.S. consumers, and each is good for specific uses. Soft or silken tofu is ideal for baking, as well as for other foods that tend to have a high water content such as smoothies, soup, and sauces. Firmer tofu varieties function well in scrambles, stir fries, and main entrees because they maintain their shape well. Less common is dried tofu, which is often seasoned and works best in savory dishes. The versatility, easy preparation, high protein content, and relatively low cost (~$2.00 per block) of tofu are what make it an appealing food choice for vegetarian and non-vegetarian individuals alike.
There are multiple opportunities for contamination of tofu along the industrial production chain. Three specific steps are taken during production to reduce the risk of microbial contamination of tofu, especially by the spore-forming bacteria that are commonly found on soybeans. First, the soybeans that arrive at tofu production plants are thoroughly washed to reduce surface pathogens. Second, the tofu is also usually pasteurized after packaging to inactivate heat-sensitive pathogens and extend the shelf-life of the product. Lastly, tofu is generally packaged in an aqueous solution containing a mixture of preservatives that help to maintain freshness and prevent microbial gas formation and contamination.
As with all foods, tofu has ideal storage conditions and shelf life recommendations. Tofu should be consumed within the stated shelf-life listed on the packaging (roughly 28 days), and it should be constantly refrigerated at under 41°F until used to reduce the risk of foodborne illness associated with C. botulinum, Staphylococcus aureus, and Salmonella typhimurium, among other pathogens. The pH of tofu changes during storage due to organic decomposition by microorganisms and can be accelerated by improper storing temperatures. Whether the pH of tofu increases or decreases from the normal ~7.0 depends on the type of microorganisms growing in the product. Microorganisms have the potential to thrive in tofu due to the high protein and moisture content, making proper storage all the more important. Spoiled tofu can be identified by a change in texture, odor, and pH.
Individuals should use caution when home-fermenting tofu due to the botulism risks associated with poor preparation technique. The World Health Organization recommends taking extra precautions in practicing proper heating and sterilization, as well as good hygiene to aid in preventing foodborne botulism.
Consumption of soy-based food products has consistently increased in the last few decades, alongside the adoption of vegetarian diets and increased availability of soy products in grocery stores. Increased interest in soy is partially attributed to nutritional studies that have found an association between soy and decreased cardiovascular disease and cholesterol levels. Additionally, with more vigorous research and food technology advancements, public awareness of the versatility and nutritional benefits of soybeans has improved. In 2013, the Soyfoods Association of North America reported that sales of soy foods in the U.S. reached $4.5 billion, a $1 billion increase in soy foods sales over the past 17 years.
Despite the U.S. being one of the leading producers of soybeans in the world, the majority of soybeans are exported, used for oil, and used for animal feed, with just 2% of protein meal from U.S. soybeans available for human consumption. When compared to populations in other countries, especially those with historically high consumption of tofu, the U.S. is significantly lower in average soy protein consumption, except within strict vegetarian communities. The mean daily intake of soy protein in Japan is about 7-10 grams. Not including vegetarians and vegans, the average consumption of soy protein in the U.S. is estimated at under three grams per day. With the increasing popularity of vegetarian and vegan diets and continued research on the benefits of soy foods, consumption of tofu and other soy products is expected to continue to increase. According to a large prospective study involving almost 100,000 Seventh Day Adventists following a strict vegan diet, the average soy intake was estimated at 13.2 grams per day—even more than among Japanese adults.
Traditionally in Chinese and Japanese populations, tofu has been used in a variety of both savory and sweet dishes including stews, stir fries, cooked in sauce, and stews. Tofu is often used in Western countries as a meat substitute in dishes that traditionally centered around animal-based protein. Additionally, softer varieties of tofu are used in desserts, smoothies, sauces, and as a replacement for soft cheeses.
Soy foods are extremely versatile and have various nutritional benefits, including high-quality protein and low carbohydrate, high calcium, and high isoflavone content. One serving size of firm tofu is approximately three ounces. It contains 70-80 calories and provides seven grams of protein. Soybeans are one of the few plant-based sources of protein, meaning that they contain all necessary amino acids for human growth that are not synthesized by the body. Soybean protein quality has been evaluated in terms of digestibility and performance in the body and found to be similar to egg and cow milk proteins, making it a high-quality protein alternative. Proteins are the main components of muscle tissue and are necessary for hormone and enzyme creation, making adequate protein consumption essential for human function. Additionally, soybeans are a good source of calcium due to a high bioavailability, and tofu in particular, with the added calcium salts for coagulation, is an excellent source of calcium. For this reason, dieticians recommend tofu as an alternative source of calcium for those with dairy allergies or vegan lifestyles. Calcium intake plays an important role in human bone strength, and lack of calcium increases risk of developing osteoporosis.
Isoflavones are a class of phytochemicals similar in structure to endogenous estrogens, and subsequently have weak hormone-like activity on cellular processes through both estrogenic and anti-estrogenic effects. They are produced almost entirely by members belonging to the Fabaceae family. Isoflavone content in soybeans differs based on the climate in which the beans were grown and the way in which they were cultivated. Due to the mild estrogenic effects, there is debate whether isoflavones yield overall positive or negative effects on humans.” Beyond protein, calcium, and isoflavones, soybeans are also a good source of unsaturated fatty acids, B vitamins, fiber, iron, and zinc, all of which are essential for good health.
Consumption of soy foods, including tofu, has been linked to various potential health benefits. Epidemiological studies looking at substituting foods rich in saturated fatty acids with soy foods have found that cholesterol levels in participants improved, and that risk for heart disease was reduced among those consuming more soy products. Further, some researchers hypothesize that the high isoflavone content in soy foods may be a key factor in the protective effects against cancer that are identified with soy food intake.
There are several misconceptions around the health effects of soy foods, despite a wealth of literature expounding the benefits. For example, because of the structural similarity between isoflavones and endogenous estrogens, there is a misconception that soy consumption can cause thyroid problems; however, data collected from over a dozen trials have shown minimal or no changes in thyroid function with increased soy intake. Additionally, there is concern over whether the high isoflavone content in soy may have an effect on estrogen pathways and sex hormone regulation, particularly in men—yet, the majority of the data collected from populations that consume large amounts of soy contest this. Cancer risk is another major concern across populations, but the European Prospective Investigation into Cancer and Nutrition Study (EPIC) found no increased risk for cancer with increased soy isoflavone intake. In general, epidemiological studies have found that soy foods offer a protective quality for women in both Asian and Western countries at risk of breast cancer.
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