Mushrooms

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Key Factspending-external-review

  • Mushrooms are a good source of B vitamins. They are also the only source of vitamin D and one of the highest sources of selenium found in the produce section.
  • Of 300 edible mushroom species, 30 have been domesticated and 10 are grown commercially.
  • Agaricus are the leading mushroom crops worldwide and accounted for approximately 97% of the total U.S. mushroom production from 2017-2018. Oyster (Pleurotusspp.) and shiitake mushrooms rank second and third respectively in worldwide production.
  • Production systems for domesticated varieties vary by type of mushroom and include both indoor and outdoor systems. Either natural or synthetic substrates may be used.
  • Wild harvest remains the largest source of commercially important mycorrhizal species (such as truffles, chanterelles, and morels), despite scientific advances in domestication.

Introduction

Mushrooms are unique in the produce section because they are fungi and not vegetables. What we typically think of as a mushroom is the fleshy, fruiting, spore-bearing body of a fungus. The mushrooms we eat are generally composed of a stipe (stem), a pileus (cap), and lamellae (gills). There are, however, many morphological varieties of mushrooms and not all varieties have these features. There are approximately 14,000 different species of mushroom, many of which are inedible.

Mushrooms form from a small structure called a primordium which grows on some type of substrate. The primordium enlarges into an egg-shaped structure composed of hyphae, called a “button.” Mycelium, called the universal veil, surrounds the button initially. As the button grows, the veil breaks. Remnants of the veil on mature mushrooms often appear as warts or may be found hanging from the cap.

The most popular species of edible mushroom, Agaricus bisporus, is sold in three different forms:  white button, cremini, and portabella. Portobella mushrooms are the mature form of the species and cremini mushrooms are simply a different pigmented variety from the white button. Other commercially available species include oyster, shiitake, chanterelle, enoki, porcini, lion’s mane, and more. In 2017-2018, there were 307 mushroom growers in the U.S. who produced nearly 917 million pounds of mushrooms worth an estimated $1.23 billion. Pennsylvania (572 million pounds) and California (95 million pounds) are, by far, the leading producers of mushrooms but it is becoming more common for small-scale producers to sell to restaurants and at farmers’ markets. In 2018-2019, approximately 390 million pounds of dried, fresh, frozen, and preserved mushrooms were imported to the U.S., primarily from Canada, Mexico and China.

Common Edible Varieties

mushrooms varieties
Images from The Mushroom Council (http://www.mushroominfo.com/varieties/).

Foodborne Outbreaks

There are few documented cases of foodborne illness due to pathogens associated with mushrooms in the U.S.

In 1989, a multistate outbreak of Staphylococcal food poisoning was associated with canned mushrooms imported from the People’s Republic of China A reported 102 people in Mississippi, New York, and Pennsylvania became ill shortly after eating products made using the canned mushrooms. Staphylococcal enterotoxin was isolated from unopened cans in several establishments. Spoilage prior to processing likely created an anaerobic environment which inhibited the normal microbiota present on mushrooms, allowing Staphylococcus aureus to grow and produce the enterotoxin. The toxin was heat stable and thus survived the canning process which kills bacteria.

A restaurant-associated outbreak of Salmonella Heidelberg was linked to improperly handled mushrooms. The previously canned mushrooms may have come in contact with raw meat and poultry products.

2020 Enoki Mushroom Multi-State Outbreak of L. monocytogenes

In March 2020, a multi-state outbreak of Listeria monocytogenes affecting 36 people was linked to enoki mushrooms, leading to 30 hospitalization and 4 deaths due to listeriosis. Enoki mushrooms are a long, thin variety of mushrooms commonly used in East Asian cuisines. Investigation into this outbreak identified Enoki mushrooms from Green Co. LTD of Korea as the source of the outbreak, which supplied mushrooms to several U.S. distributors. Further investigation of Green Co. LTD found the enoki mushrooms imports to test positive for L. monocytogenes. Subsequently, a recall was issued in April 2020 on cases of enoki mushrooms distributed by Sung Hong Foods, Inc, Guan’s Mushroom Co., and H&C Foods, Inc. Import Alerts were additionally placed on Green Co. LTD to flag imports for inspection and examination.

Production

The general process for farming mushrooms involves six sequential steps, outlined below for the Agaricus species. The process is similar for other species, with the following slight process differences by species.

Oyster mushrooms are farmed by a similar process but require more humidity and fresh air and grow in tubular plastic bags rather than horizontal racks. Shiitake mushrooms are farmed using either natural oak logs or synthetic “logs” made from oak sawdust packed in poly bags. Enoki mushrooms are farmed in plastic bottles at colder temperatures (45°F) and only produce one set of fruiting bodies per crop. Beech mushrooms are farmed similarly to Enoki mushrooms but at higher temperatures (60-64°F). Maitake mushrooms are farmed on synthetic “logs”, similar to shiitake mushrooms, and only produce one set of fruiting bodies per crop.

  1. Phase I Composting – Making the compost:

    • The first phase of composting begins by mixing and wetting the bulk compost ingredients on a large concrete slab called a wharf. Bulk compost ingredients may be natural (manure) or synthetic. Compost can include straw, peat moss, soybean or canola meal, chicken manure, horse bedding straw, grape must from wineries, potash, urea, ammonium nitrate, and/or lime. Nitrogen and gypsum supplements are added by topdressing the compost pile. A compost turner is used to mix and aerate the compost, and water is added as the bulk ingredients are mixed. The mixture is then stacked in piles with tight sides and loose centers, or ricks. Resulting conditions favor the growth of naturally occurring aerobic microorganisms, which produce heat through aerobic fermentation. Turning the hot (145°F – 175°F) compost pile regularly prevents conditions favoring the growth of anaerobes. Phase I composting usually occurs outdoors and takes 7-14 days to complete depending on the material used at the start.
  2. Phase II Composting – Finishing the compost:

    • During this phase, which lasts 10-14 days, the compost is pasteurized to kill any pests present in the compost and remove ammonia formed during Phase I composting. High-temperature and low-temperature protocols are available. In the high-temperature protocol, the compost is heated to >145°F for 6 hours either through the naturally occurring heat produced by microorganisms or through added steam. After 6 hours, the temperature is lowered to 140°F, then the compost is allowed to cool at a rate of 2-3°F per day until the ammonia is dissipated. During the low-temperature protocol, the compost is heated to approximately 126°F using the same methods as in the high-temperature protocol, then the temperature is lowered by about 2°F a day for 4-5 days until the ammonia is dissipated. By the end of Phase II, the compost temperature must be lowered to 75 to 80°F before spawning can begin. Pasteurization is typically computer controlled, closely monitored, and well documented.
  3. Spawning:

    • During this phase, the compost is inoculated with commercially produced mycelium (mushroom spawn) and held under controlled conditions to allow the spawn to colonize the substrate. The spawn will be evenly distributed throughout the compost while the compost temperature is held at 75°F and humidity is kept high, which allows the spawn to grow. This period, called the spawn run, generally takes 14-21 days.
  4. Casing:

    • In this step, casing (a top-dressing of clay-loam field soil mixed with peat moss, ground limestone and, occasionally, spent, reclaimed mushroom substrate) is applied to the spawn-run compost and the crop is heavily watered. The casing acts as a water reservoir and is where thicker mycelia (called rhizomorphs) form. After casing, the compost is kept at approximately 75°F for 5 days with high relative humidity, then the temperature is lowered by 2°F per day until young mushrooms (pins) form. Although casing may be pasteurized either on farm or by commercial suppliers prior to receipt, recent research suggests that pasteurization of casing may not be beneficial as it may destroy microorganisms that competitively inhibit the growth of Listeria 
  5. Pinning:

    • When the rhizomorphs change from the vegetative growth stage to the fruiting growth stage, young mushrooms, called pins, push up through the casing layer. Pins develop in response to the introduction of fresh air into the growing room, which lowers the ambient concentration of carbon dioxide. The timing of fresh air introduction affects both yield and quality of the harvest and is best performed when the mycelium shows on the surface of the casing.
  6. Cropping:

    • During this phase, mature mushrooms are harvested in 3-5-day periods called “breaks.” A complete harvest usually takes 30-42 days but can go on for up to 150 days. Air temperature during cropping is held between 57°F and 62°F to favor growth, however these temperatures may lengthen the life cycle of pathogens and pests.

Post-Harvest

Packaging methods for mushrooms can vary between farms, however fresh mushrooms should be refrigerated at 35° to 45°F. To limit spoilage and bacterial growth, mushrooms require a complete cold chain for storage and transport.  Additionally, mushrooms should have adequate ventilation to prolong shelf life and should not be stored in unperforated plastic. Breathable pulp-trays are common for commercial mushrooms sales which allow for ventilation. When held within these conditions and packaged properly, the typically shelf life of mushrooms is 7-10 days.

Food Safety

There are several pathogens that are of concern in mushroom production. Campylobacter, a leading cause of bacterial enteritis, was isolated from mushrooms sampled in retail markets. Clostridium botulinum is of particular concern in mushroom production and improper home preservation has been linked multiple times to illness and death. The spore-forming bacterium can thrive in improperly packaged mushrooms. Mushrooms’ high rate of respiration can rapidly create an anaerobic environment within sealed plastic packages which favors growth of C. botulinum and, ultimately, production of botulinal toxin. The general recommendation for consumers is to store mushrooms in the refrigerator, unwashed in a paper bag, to prevent trapping moisture which will promote spoilage.

Basket of wild edible mushrooms
Wild edible mushrooms. Photo by Carl F. Bagge.

Wild Mushrooms

The vast majority of food illness associated with mushrooms is from the consumption of wild picked mushrooms. Wild mushrooms may contain several toxins, such as muscimol and muscarine, which can cause vomiting, diarrhea, confusion, visual disturbances, salivation, and hallucinations. Some mushrooms even contain toxins which can cause hepatic and renal failure, leading to death. Domestic, farm-raised mushrooms are usually a safe and nutritious food; wild mushrooms, however, should only be consumed under the guidance of a trained mycologist or mushroom expert who meets criteria required for wild mushroom identification by state or local health departments. Cooking or drying cannot reduce the toxicity of poisonous mushrooms.

Consumption Mushrooms sauteed in a skillet

In the United States, the most popular varieties of mushrooms include the “whites” (Agaricus), criminis, portabellas, and shiitakes. From 2007 to 2015, the Americans annual consumption of mushrooms has stabilized at an average of 3 pounds of mushrooms per person. Of the total amount, 2.2 pounds were fresh mushrooms and 0.8 pounds were processed mushrooms. In the 2006-2007 Population Atlas Survey of Exposures, 33.5% of the survey cohort reported eating fresh mushrooms within the past 7 days. There is growing appeal of mushrooms for their nutritional properties and culinary attributes.

Culinary Attributes

Mushrooms are commonly consumed throughout the U.S. in dried, raw, and cooked forms. White button mushrooms are often added to soups, salads, and pizzas. Portabella mushrooms are common in Italian cuisines, added to sauces and pasta dishes. Additionally, portabellas are used as meat substitute for its umami flavor and texture. Similarly, dried shiitakes are often added to dishes to add umami and an intense savory flavor. East Asian cuisine often include various mushrooms, such as oyster, enoki, and shiitake, in sauces, soups, stir-fries, and other dishes.

Information on storing mushrooms safely can be found at FoodKeeper App.

Nutrition

Nutritionally, mushrooms are often grouped with produce, but they add some nutrients not found or found in limited amounts in other produce. 100 grams of raw mushrooms have only 22 calories, no fat, and provide 3 grams of protein, 3 grams of carbohydrate, and 1 gram of dietary fiber. They are often marketed as a “meat replacer” due to their protein content and fleshy texture. Notably, mushrooms exposed to UV radiation synthesize vitamin D2, making mushrooms the only known nonanimal source of dietary vitamin D. Mushrooms are also a good source of the B vitamins riboflavin, pantothenic acid, and niacin. They provide several important minerals such as selenium, ergothioneine, copper, and potassium.

In addition to these nutritional components found in mushrooms, they also a source of bioactive compounds associated with positive health effects. These bioactive compounds include secondary metabolites, such as polyphenols and alkaloids, polysaccharides, volatile fatty acids, and bioactive proteins.  A wide variety of mushrooms, over 100 species, have been utilized in traditional medicines for medicinal uses such as anti-neoplastic, antioxidant, antiallergic, and antimicrobial properties. Such functional properties of mushrooms represent an ongoing area of research investigating potential roles of mushroom phytochemicals on health and disease prevention.

References

  1. Barney DL. Growing Mushrooms Commercially – Risks and Opportunities [Internet]. University of Idaho College of Agriculture; Available from: http://col.st/1l5Hxsy
  2. Beetz A, Kustudia M. Mushroom Cultivation and Marketing [Internet]. National Sustainable Agriculture Information Service. 2013 [cited 2014 Jun 10]. Available from: http://col.st/1l5IAc6
  3. Centers for Disease Control and Prevention. Epidemiologic Notes and Reports Multiple Outbreaks of Staphylococcal Food Poisoning Caused by Canned Mushrooms. MMWR. 1989 Jun 23;38(24):417–8.
  4. Doyle MP, Schoeni JL. Isolation of Campylobacter jejuni from retail mushrooms. Appl Environ Microbiol. 1986 Feb;51(2):449–50.
  5. Horwitz M, Marr J, Merson M, Dowell VR, Ellis J. A continuing common-source outbreak of botulism in a family. The Lancet. 1975;306(7940):861–863.
  6. Hoyle S. Mushrooms Profile [Internet]. Agricultural Marketing and Resource Center. 2014. Available from: http://col.st/lXRLG
  7. Miles PG, Chang S-T. Mushrooms: Cultivation, Nutritional Value, Medicinal Effect, and Environmental Impact [Internet]. Second Edition. CRC Press; 2004 [cited 2014 Jun 10]. 480 p. Available from: http://col.st/1l5NANN
  8. Mushroom Council. Fresh Mushrooms – Nature’s Hidden Treasure [Internet]. [cited 2014 Jun 10]. Available from: http://col.st/1l5LhKy
  9. Nutrition C for FS and A. Outbreak Investigation of Listeria monocytogenes: Enoki Mushrooms (March 2020). FDA [Internet]. 2020 May 4 [cited 2020 Jun 2]; Available from: https://www.fda.gov/food/outbreaks-foodborne-illness/outbreak-investigation-listeria-monocytogenes-enoki-mushrooms-march-2020
  10. Sugiyama H, Yang KH. Growth potential of Clostridium botulinum in fresh mushrooms packaged in semipermeable plastic film. Appl Microbiol. 1975 Dec;30(6):964–9.
  11. The American Mushroom Institute. Welcome to American Mushroom Institute [Internet]. American Mushroom Institute. 2014 [cited 2014 Jun 10]. Available from: http://col.st/1l5GB7z
  12. U.S. Army. Department of Defense Military Handbook: Guidelines for Auditing Food Establishments [Internet]. EverySpec. 2008 [cited 2014 Jun 10]. Available from: http://col.st/1l5QBh6
  13. United States Department of Agriculture. Mushrooms [Internet]. United States Department of Agriculture; 2018. Available from: http://col.st/1l5Ofic
  14. University of Kentucky Cooperative Extension Service. Truffles & Other Edible Mycorrhizal Mushrooms [Internet]. University of Kentucky Cooperative Extension Service; 2012. Available from: http://col.st/1l5KpWs
  15. USDA – Economic Research Service. Data by Commodity – Imports and Exports [Internet]. [cited 2020 Jun 2]. Available from: https://data.ers.usda.gov/reports.aspx?programArea=veg&stat_year=2007&top=5&HardCopy=True&RowsPerPage=25&groupName=Vegetables&commodityName=Mushrooms&ID=17858#P336dbfe855f94c578c93c5239a63dc73_5_292
  16. Valverde ME, Hernández-Pérez T, Paredes-López O. Edible Mushrooms: Improving Human Health and Promoting Quality Life. Int J Microbiol [Internet]. 2015 [cited 2020 Jun 2];2015. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4320875/
  17. Weidenbach KN. Restaurant-associated outbreak of Salmonella serotype Heidelberg linked to improperly handled mushrooms, Wyoming, 2003. Food protection trends. 2006 Mar;26(3):150–7.

Authors

Daren Harrison

Daren Harrison

Marisa Bunning

Marisa Bunning

Lauren Pecher

Lauren Pecher