Peanut and Peanut Products: a Food Safety Perspective

Food Control 32 (2013) 296e303

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Food Control

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Review Peanut and peanut products: A food safety perspective

Alexandra S. Chang a, Aswathy Sreedharan b, Keith R. Schneider b,* a Land O’Lakes, Inc. P.O. Box 64101, MS 0075, St. Paul, MN 55164-0101, USA b Food Science and Human Nutrition Department, University of Florida, 359 FSHN Bldg., Newell Drive, Gainesville, FL 32611-0370, USA article info abstract

Article history: Peanuts are a common food allergen. The increased prevalence of peanut food allergy in recent years has Received 14 October 2011 led food processors to be more proactive in their responsibility for preventing peanut contamination by Received in revised form implementing good manufacturing practices (GMPs) and allergen control programs. Further, safety of 3 December 2012 peanuts and peanut-derived products must be considered throughout production to minimize risk of Accepted 8 December 2012 foodborne disease. Peanuts can be a source of aflatoxin, produced by the mold Aspergillus spp., the cause of liver defects and cancer, especially in developing countries. Though historically not associated with Keywords: foodborne disease outbreaks, recent events have put peanut products in the limelight. Perhaps the most Peanuts Peanut butter well-known peanut-related food safety issue has been the peculiar relationship between peanut butter Aflatoxin and Salmonella. Though there have only been a few outbreaks caused by Salmonella in peanut butter, they Allergen have been prominent and widespread. The costly multistate outbreak of 2009 involving a Georgia peanut Salmonella manufacturer influenced recognition of the importance of corporate responsibility and GMPs. [Federal regulations to help prevent such outbreaks have also been developed including the proposed Food Safety Modernization Act of 2011.] Prevention of outbreaks is best accomplished through cooperation within the food industry community and with regulators to implement effective GMPs and other prevention- based food safety programs. These, and other peanut food safety issues are discussed in this review. Ó 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction ...... 297 2. Peanuts ...... 297 2.1. Production ...... 297 2.2. Areas of concern ...... 297 2.2.1. Allergens in food processing and product formulation ...... 297 2.2.2. Mycotoxins ...... 298 2.2.3. Cross contamination and pathogen survival ...... 299 2.2.4. Peanut outbreaks ...... 299 3. Peanut products ...... 299 3.1. Peanut oil ...... 299 3.2. Peanut butter ...... 300 3.2.1. Salmonella ...... 300 3.2.2. Control technologies ...... 300 3.3. Peanut-derived products ...... 301 4. Conclusions ...... 301 References ...... 301

* Corresponding author. Tel.: þ1 352 392 1991x309; fax: þ1 352 392 9467. E-mail address: keiths29@uﬂ.edu (K.R. Schneider).

1. Introduction peanut plant produces flowers. Pods containing one to three seeds develop in branches and are pushed underground where they Peanuts (Arachis hypogaea) are an inexpensive, nutritionally mature. Branch-type peanuts grow closely in clusters at the bottom powerful food source for people worldwide (Reese & Lehrer, 1999). of branches while runner-type peanuts grow pods throughout the Over one billion pounds of peanuts are produced annually in the US branches (Woodroof, 1983). alone, most of which remains in the country for human Woodroof (1983) describes the following process for peanut consumption. Peanuts are consumed whole roasted and as a variety production. Peanuts are harvested by mechanical inverting, of products including peanut butter, peanut oil, and other forms as digging, then picking. At digging, peanuts are at 35e50% moisture. ingredients. Improved diet nutrient profiles and lower body mass Entire plants are removed from the ground and formed into index (BMI) have been linked to eating peanuts (Griel, Eissenstat, windrows, which are dried in open air. After a specific time, Juturu, Hsieh, & Kris-Etherton, 2004). Though they are energy- peanuts are mechanically picked and brought to a processing dense, peanuts provide satiety, low energy absorption, and facility where they are dried by fan at 35 C (95 F) to 10% moisture. increased energy expenditure after consumption so that they do Peanuts are allowed to mature as determined by the internal not significantly contribute to increased body weight (Mattes, Kris- surface color of shell of a representative sample. During cleaning, Etherton, & Foster, 2008). Given the health benefits and scope of dirt, stones, plant material, and other debris are removed by peanut consumption worldwide, it is important that consumers are screens and blowers. Peanuts can also be stored under conditions able to enjoy a safe peanut supply. that maintain moisture below 10%. Temperature should be main- Peanut is one of the eight most common food allergens. The tained between 0 and 10 C (32e50 F). If shelled, peanuts must be increased prevalence of peanut food allergy in recent years has led stored at a lower relative humidity to maintain low moisture food processors to be more conscientious in their good content. Shelled peanuts can be stored a maximum of 18 months manufacturing practices (GMPs) and allergen control programs to compared to 24 months for in-shell peanuts. prevent peanut contamination. Further, safety of peanuts and The critical control point in peanut processing is roasting, which peanut-derived products must be considered throughout produc- can be performed in two ways, dry and oil roasting. In dry roasting, tion for foodborne disease risk. While they have not been associ- peanuts reach 160 Cinanovenof>400 C for 25e60 min (roasting ated with many foodborne disease outbreaks, peanuts can be times vary based on batch properties and final product character- a source of aflatoxin, produced by the mold, Aspergillus spp., which istics desired). Peanuts are then cooled slightly and undergo can cause liver defects and cancer, especially in developing coun- a blanching process, where peanut skins, dust and other foreign tries (Wild & Gong, 2010). More recently, peanut butter has been in materials are blown off. In oil roasting, peanuts are blanched and the spotlight as the source of foodborne disease outbreaks caused then fried at 140 C for 3e10 min. Roasted peanuts have approxi- by Salmonella (CDC, 2007; 2009). In light of the 2009 multistate mately 1.25% moisture content (Woodroof, 1983). outbreak involving numerous peanut products from a Georgia peanut manufacturer, corporate responsibility and GMPs are being 2.2. Areas of concern increasingly recognized and important (US FDA, 2009a). Federal regulations to prevent such outbreaks have also been developed. Consumption of peanuts and peanut products can induce This review article will provide an overview of major safety potential life threatening anaphylactic reactions to individuals who concerns in peanut and peanut products production. are allergic to peanuts. Currently, since there are no effective curative treatments available, the most effective way to deal with 2. Peanuts peanut allergies is to strictly avoid peanut and peanut products. However, accidental exposures are frequent due to the possibility of 2.1. Production cross contamination of other foods. Hence, it is imperative that the food processing industries follow strict guidelines to ensure that Peanuts, also known as a goober, groundnut, earthnut, and the food prepared is safe for allergic consumers, by following good pinder, among other names, originated in South America around 950 manufacturing practices to reduce cross contamination, and by BC. Peanuts were brought to Africa by early explorers, who then including proper advisory labeling on packages. transported them to North America in the colonial age. Peanuts were Peanuts do not pose a large risk for foodborne disease largely first used primarily as animal feed and human consumption began due to the roasting step where peanuts are reduced to the 1.25% only in the late 19th century (Woodroof, 1983). Today, the average moisture content and <0.75 water activity (aw). Moisture is American consumes approximately 6.4 lbs of peanuts a year, about required for most microorganisms to survive. The low aw inhibits half of which is in the form of peanut butter (USDA 2010). growth of most bacteria and many molds. Since peanuts are rarely World production of peanuts is estimated at 40 billion pounds eaten raw, roasting not only improves peanut aroma, flavor, and (Woodroof, 1983). The US comprises about 10% of world produc- texture, but also destroys contaminating microorganisms tion, producing approximately 4.2 billion lbs in 2010 with a value of (Woodroof, 1983). over $900 million (USDA, 2011a; b). Value increased over $100 Very few outbreaks of foodborne diseases have been attributed million from 2009, but in previous years the peanut industry ach- to whole peanuts and any outbreaks that have occurred were likely ieved over $1 billion in sales (USDA, 2011b). Georgia is the number due to poor handling practices after a thermal treatment step, one producer of peanuts, comprising almost half of US production particularly roasting. Proper peanut processing and handling post- and value. In total, over one million acres of peanuts are planted harvest should ensure a safe product for consumers. Instead, from and harvested in the US each year (USDA, 2011a; b). Approximately the foodborne diseases perspective, areas of concern for peanuts 60% of total production is dedicated for human consumption and revolve primarily around contamination from aflatoxin, a myco- the remaining is used for seed, animal feed, and oil. Of the peanuts toxin produced by the mold Aspergillus, and cross contamination used for human consumption, approximately 63% is processed into from sources that introduce pathogens to peanuts after processing. peanut butter (Woodroof, 1983). Peanuts are the fruit or pod of annual legumes, the plants 2.2.1. Allergens in food processing and product formulation belonging to the family Leguminosae. Legumes also include peas, Peanut is one of eight major food allergens of humans, which beans, and soybeans (Reese & Lehrer, 1999). The central stem of the also include milk, egg, soy, wheat, tree nuts, fish, and shellfish. 298 A.S. Chang et al. / Food Control 32 (2013) 296e303

Estimated prevalence of food allergies among adults in North distribution of peanuts. Furthermore, a restriction would be America is 3e4% (Sicherer & Sampson, 2010). In 2007, the Centers unenforceable and there was lack of evidence if a buffer zone would for Disease Control and Prevention (CDC) reported approximately be effective considering peanut residue from previous flights 3.9% (3 million) children in the US had food allergies (Branum & (Federal Register, 2011). Despite the lack of action here, concern for Lukacs, 2008). From 1997 to 2007, prevalence of food allergy allergic individuals had instigated the US Congress to pass the Food increased 18% among children. Additionally, hospitalizations Allergen Labeling and Consumer Protection Act in 2004 requiring related to food allergies have increased, and children with food food packages, if not otherwise obvious, to be labeled if they con- allergy were more likely to report having asthma. A more recent tained one of the eight major food allergens (Public Law, 2004). study reported a higher prevalence of food allergies, at 8.0% of Labeling mistakes still occur, however. In 1999, 236 food products children in the US, 25.2% of which were allergic to peanut (Gupta were recalled due to undeclared allergens, most commonly because et al., 2011). Kotz, Simpson, and Sheikh (2011) reported preva- of ingredient omission or error and cross contamination (Vierk, lence of peanut allergy in children in the US to be 0.4e1.9%. Falci, Wolyniak, & Klontz, 2002). Thirty five of the recalled prod- A food allergy is generally described as an adverse reaction to ucts had undeclared peanuts. The most common types of food food (Bischoff & Sellge, 2003). Immunoglobulin E (IgE) mediated recalled were candy and bakery items (Vierk et al., 2002). food allergy, also known as type I hypersensitivity, is considered Food allergens are chemical hazards. The increasing prevalence a true food allergy as it elicits an immune response after multiple of food allergies, whether or not due to an actual increase or simply exposures to an allergen. Food allergens are antigens or proteins an increase in awareness, inspires consumers to be more assertive with which antibodies in the human body bind. The initial expo- in demanding safe food. Vierk et al. (2002) reported that in their sure to an antigen is known as the sensitization phase in which no examination of food recalls in 1999, consumers were responsible symptoms occur but specific IgE antibodies that can bind to the for identifying the presence of an allergen in 56% of food products antigen are produced in larger quantities (Bischoff & Sellge, 2003). recalled due to undeclared allergens. Food producers are thus Subsequent exposure to the antigen causes mast cells, basophils, becoming more vigilant in GMPs and control methods to prevent and eosinophils to degranulate, releasing prostaglandins, leuko- cross contamination (Taylor & Hefle, 2005). Control measures trienes and other immune mediators. Inflammatory reactions include labeling all raw materials and ingredients, separation of caused by immune mediators vary in severity, but can include allergenic materials, dedication of equipment, scheduling, proper a tingling sensation around the mouth, urticaria, rhinitis, asthma, sanitation, sanitation validation, and effective packaging. Effective anaphylactic shock, and death within an hour of exposure (Branum allergen control programs can reduce number of allergen-related & Lukacs, 2008; Reese & Lehrer, 1999). recalls and incidences leading to hospitalization or death. Peanut is often considered the most severe allergen, the major allergens being Ara h 1 and Ara h 2, of 63.5 and 17.0 kD molecular 2.2.2. Mycotoxins weight, respectively (Reese & Lehrer, 1999). The threshold at which Mycotoxins are produced by various fungi and are considered allergic individuals experience symptoms is measured by the poisonous contaminants in susceptible foods and feeds. Aflatoxin Lowest Observed Adverse Effect Level (LOAEL). The range of LOAEL has been identified as the most toxic mycotoxin associated with doses in clinical trials has ranged from 0.5 to 10,000 mg of whole peanuts, and hence the toxicity, and measures to manage and peanut, indicating high variation in allergic response in a pop- prevent contamination by aflatoxin has been discussed in detail in ulation. A dose predicted to provoke a reaction in 10% of the peanut this review. In addition to aflatoxins, another commonly occurring allergic population was estimated to be 18.0 mg of whole peanut natural contaminant of peanut is the mycotoxin cyclopiazonic acid, (Taylor, Crevel, Sheffield, Kabourek, & Baumert, 2009). produced by several species of Penicillium and Aspergillus (Lansden The increasing prevalence of peanut allergy has garnered & Davidson, 1983). Cyclopiazonic acid is a potent inhibitor of the þ scientific attention. One study noted the lower prevalence of reticular form of the Ca2 ATPase pump (Plenge-Tellechea, Soler, & peanut allergy in China compared to in the US, perhaps because Fernendez-Belda, 1997). The compound is not considered to be peanuts are usually fried or boiled instead of roasted (Beyer et al., a potent toxin in humans due to low oral LD50 values, in the range of 2001). Researchers found fried and boiled peanuts to contain less 30e70 mg/kg in rodents (Antony, Shukla, & Janardhanan, 2003; Ara h 1 and elicit less IgE binding of Ara h 2 and other allergens Nishie, Cole, & Dorner, 1987). On peanuts, the natural level of compared to roasted peanuts. Newer technologies such as pulsed contamination by this toxin is only 6.5 ppm (Lansden & Davidson, ultraviolet light, gamma irradiation, treatment with polyphenol 1983), thus, the compound is toxic to humans only when it is oxidase and phenolic compounds to crosslink proteins, and consumed at levels that exceed the natural level of intake of the genetically modifying peanut plant genes have shown to be effec- toxin (Burdock & Flamm, 2000; Van Rensburg, 1984). Further, in tive against certain peanut allergens, though additional studies are most cases, both cyclopiazonic acid and aflatoxin, both produced by needed to demonstrate clinical significance and practicality Aspergillus flavus, are present concurrently (Urano et al., 1992), and (Chung, Kato, & Champagne, 2005; Chung, Yang, & Krishnamurthy, this effectively disguises the presence of cyclopiazonic acid. A study 2008; Dodo, Konan, Chen, Egnin, & Viquez, 2008; Lee, Oh, Jang, Lee, conducted by Van Rensburg (1984) concluded that in the presence & Byun, 2008). of usual hygiene and aflatoxin control practices in peanuts, no Recognition of peanut allergy also reached the federal govern- further control or screening measures for cyclopiazonic acid is ment. Among the US Department of Transportation (DOT) warranted. proposals in 2010 was one to accommodate individuals with severe Although to a much lesser extent, there are also reports of peanut allergy by prohibiting the serving of peanuts, or creating natural occurrence of other mycotoxins associated with peanuts, a peanut-free buffer zone on commercial airlines (Federal Register, including zearalenone (El-Maghraby & El-Maraghy, 1987; Kishore, 2011). The concern was that airborne peanut particles in the Pande, Manjula, Rao, & Thomas, 2002; Mehan & McDonald, 1982), enclosed cabin could induce an allergic response in individuals and trichothecene-toxins (Bhavanishankar & Shantha, 2006; El- with severe allergy. Due to responses gathered during the comment Maghraby & El-Maraghy, 1987), both produced by Fusarium sp.; period, however, the DOT did not take further action, citing conflict citrinin (El-Maghraby & El-Maraghy, 1987; Subrahmanjan & Rao, with Public Law 106-69. The Law prohibits use of funds available 1974), produced by Penicillium sp., Aspergillus sp. and Monascus under the DOT and Related Agencies Appropriations Act of 2000 to sp.; and ochratoxin A (Magnoli et al., 2007) produced by Asper- require air carriers to provide a peanut-free buffer zone or restrict gillus sp. A.S. Chang et al. / Food Control 32 (2013) 296e303 299

Aflatoxin is identified as a known human carcinogen by the 2.2.3. Cross contamination and pathogen survival International Agency for Research on Cancer (2002),p.301.A. flavus Implementation and adherence to good agricultural practices and Aspergillus parasiticus (commonly found in the soil) are the (GAPs) and GMPs should prevent contamination and foodborne primary species of mold that produce aflatoxin as a secondary diseases caused by peanuts. What becomes a concern is the survival metabolite. Originally discovered in the 1960s, aflatoxin is one of of pathogens should cross contamination occur, post-harvest and/ several mycotoxins that persist in peanuts, tree nuts, oilseeds, and or post-processing. Cross contamination can occur anytime during cereal grains, especially in developing countries where these peanut production and turn a low moisture, safe food into one that commodities are grown and consumed (Wild & Gong, 2010). can cause foodborne disease. Pathogens can be transferred in Optimal conditions for A. flavus growth are 12e35% moisture at several ways to food, such as through contaminated water and 27e38 C (80e100 F) (Woodroof, 1983). Once infected, the mold equipment, poor worker hygiene, and pests. If peanuts are can proliferate in improperly stored peanuts, particularly in tropical contaminated, survival of pathogens becomes a major issue. regions. It is generally understood that low aw of a food prevents growth The types of aflatoxin are B1, B2, G1, and G2 (IARC, 2002, p. 301). of many microorganisms. To verify the low association of pathogens Aflatoxin B1 is the most ubiquitous form and the most toxic and peanuts, Eglezos (2010) tested 343 samples of ready-to-eat (Kamika & Takoy, 2011; Wild & Gong, 2010). Major effects of afla- peanuts and samples of other nuts produced at Australian facility toxin are hepatocarcinoma, immunosuppresion leading to over three years for Salmonella, other pathogens, and aerobic plate increased susceptibility to infections, and growth impairment in count (APC). No pathogens were found in any sample. In this study, children due to the ability of aflatoxin to cross the human placenta APC tests revealed that 48% of the peanut samples show counts (IARC, 2002, p. 301). Incidentally, chronic hepatitis B and hepatitis C above the detection limit of 100 CFU/g. These positive samples had infection are risk factors for hepatocarcinoma caused by aflatoxin average plate counts of 2.7 log CFU/g. High APC counts do not (Bhat, Rai, & Karim, 2010). It is hypothesized that the viral infections necessarily indicate the presences of a foodborne pathogen, but interfere with the ability of hepatocytes to metabolize aflatoxin. instead, are a general indicator of sanitation and can assist peanut The toxin resides in the liver for a longer period, causing damage to processors in identifying where sanitation can be improved. tumor suppressor genes. An immediate consequence of aflatoxin Dry foods like peanuts do not often support microbial growth, but exposure can be aflatoxicosis, or aflatoxin poisoning. Signs and they may still be able to allow survival of pathogens. Komitopoulou symptoms include gastrointestinal problems and liver lesions (Bhat and Penaloza (2009) found that inoculated Salmonella could survive et al., 2010). Exposure to amounts less than 1000 ppb have been for 3e4 weeks on dry, raw materials including crushed cocoa and linked to aflatoxicosis. Consuming approximately 5000 ppb of hazelnut shells, cocoa beans, and almond kernels at both room aflatoxin can cause acute aflatoxicosis leading to death. The LD50 temperature and 5 C. Salmonella is typically inhibited by aw < 0.91, value of aflatoxin ranges from 0.3 to 10 mg/kg for most animal but the aw of these substances were likely much lower. It can be species, and from 0.54 to 1.62 mg/kg for human beings (Wild & concluded that any heat treatment of food must be sufficiently high Gong, 2010). to destroy Salmonella while still providing a quality product. This is Aflatoxin content in peanuts is controlled. In the US, aflatoxin especially important for dry foods with long shelf life because if content in peanuts must be < 15 ppb to be certified edible quality pathogens were to survive during processing, they would more grade (CFR, 2010a). The Food and Drug Administration (FDA) will likely reach the consumer and increase risk of disease. pursue legal action if peanut and peanut products are found to contain at least 20 ppb aflatoxin (US FDA, 2000). It is a common 2.2.4. Peanut outbreaks difficulty to obtain a representative sample from a truckload of Foodborne disease outbreaks are not typically associated with peanuts for testing, however (Doughtie, 1947). Representative peanuts and very few peanut outbreaks have been documented. In sampling of peanuts is important because of non-uniform distri- one international outbreak, Salmonella Stanley, S. Newport and bution of aflatoxin in a batch of peanuts. The level of contamination other strains were found in packages of a brand of roasted, in-shell can also vary. Specific guidelines for acceptable levels of aflatoxin in peanuts imported from Asia from May to October 2001 (Kirk et al., food and feed, and sampling plans for sample acceptance or 2004). There were 109 cases total in Australia, Canada, England, rejection have been established by different countries (Van Wales, and Scotland. Positive samples were found to contain Egmond, 1989; Whitaker, Springer, Defize, DeKoe, & Coker, 1995). <0.03e2 CFU/g Salmonella. The peanuts were manufactured in one In the US, the peanut marketing agreement established by the unidentified Asian country and distributed by several other coun- USDA, is administered by the Peanut Administrative Committee tries. The original source of contamination was undetermined (Kirk (PAC). According to the current aflatoxin sampling plan followed in et al., 2004). the US, raw shelled peanuts are accepted or rejected based on The first Salmonella outbreak in the US associated with boiled a modified sequential plan where up to three 21.8 kg each repre- peanuts occurred in 2006 at the Pumpkin Festival in Pumpkintown, sentative test samples are drawn from a single lot (Whitaker & SC. Twenty three cases were reported. While boiling should destroy Dowell, 1995; USDA, 2004). Peanuts are finely ground into any vegetative microorganisms in peanuts, in this outbreak, a composite since aflatoxin can exist on the order of parts per contamination by S. Thompson occurred after boiling and salting. billion. Prevention of Aspergillus growth by effectively drying and Poor handling, inadequate temperature control, and possible ladle storing peanuts at low relative humidity and temperature is the contamination all could have been prevented by following proper best way to prevent aflatoxin production. Genetically modified food service procedures (Christian et al., 2007). Other documented seeds resistant to Aspergillus have been developed but are expen- outbreaks have been associated with peanut products, especially sive (Wild & Gong, 2010). If peanuts are contaminated, various peanut butter, and are described in section 3.2.1 and 3.3. treatments exist such as applying ammonia, hydrogen peroxide, and ozone, although the side effects of these treatments are not 3. Peanut products currently reported in detail (Bhat et al., 2010; Scott, 1998). Irradi- ation and high temperature roasting can also eliminate aflatoxin 3.1. Peanut oil contamination (Bhat et al., 2010; Ogbadu, 1980; Staron, Thirouin, Perrin, & Frere, 1980). With ongoing research, many of these About two-thirds of the world peanut crop is used for oil. In the options may become more cost effective in the future. US, peanut oil is primarily used as cooking oil or salad oil 300 A.S. Chang et al. / Food Control 32 (2013) 296e303

(Woodroof, 1983). The oil extraction process begins with hydraulic a leaky roof of a Sylvester, GA processing plant. In total, 628 people pressing where peanuts and shelled, crushed, heated with steam were infected in 47 states. Age of patients ranged from two months and spread on press cloths. Peanuts are pressed under 14,000 psi. to 95 years and 20% of infected individuals were hospitalized (CDC, The resulting crude oil undergoes solvent extraction, refinement, 2007). The manufacturer took steps to prevent future outbreaks by water washes, and bleaching (Parker & Melnick, 1966). redesigning the plant, installing new equipment, and appointing There is no true standard of identity for peanut oil, but it can be a food safety advisory committee (ConAgra Foods, Inc., 2007). described as composed of 100% fat with trace minerals and no A complex, multistate outbreak in 2009 was caused by Salmo- detectable macromolecules. Refined peanut oil is not allergenic to nella typhimurium associated with peanut butter and peanut people with peanut allergy since oil should not contain any protein products produced by a Georgia peanut manufacturer. They man- (Taylor, Busse, Sachs, Parker, & Yunginger, 1981). Hourihane, ufactured peanut butter sold in bulk to institutions, food service Bedwani, Dean, and Warner (1997) found that when 60 individ- and private label companies. The first suspected product that was uals allergic to peanuts were exposed to refined peanut oil, no the common food consumed by infected patients was a brand of allergic reactions occurred. Ten percent of subjects did experience peanut butter produced at the GA plant (CDC, 2009). Peanut butter a reaction when exposed to crude peanut oil however, which is and other peanut products were used as ingredients in numerous known to contain protein. While allergic individuals should be able other products. In total, over 3900 products were recalled from over to safely use refined peanut oil, there may be little control by 200 companies. The outbreak caused 714 cases in 46 states and 1 in patrons for preventing cross contamination in restaurants where Canada, 171 hospitalizations and 9 deaths (CDC, 2009). peanut oil is often used for frying. Foods containing peanut protein These high-profile outbreaks will associate Salmonella with placed in oil may be transferred to non-allergenic food fried in the peanut butter for years to come. Many peanut butter companies same oil afterward. likely adopted Salmonella and other pathogen testing as part of Aflatoxins are primarily a problem for whole peanuts, not their routine microbiological testing. In March 2011, the FDA issued peanut oil. In one study, peanut oil extracted from peanuts a recall of a reduced fat peanut butter spread because of possible contaminated with 5500 ppb aflatoxin resulted in a final product contamination with Salmonella (US FDA, 2011b). Salmonella was with <1 ppb aflatoxin (Parker & Melnick, 1966). Peanut oil found in the finished product as part of the company’s routine produced and used in developing countries, however, may be of testing program, though no illnesses had been reported. higher risk. For example, researchers studying the high incidence of hepatocellular carcinoma in a rural farming community in China 3.2.2. Control technologies detected aflatoxin in peanut oil. Of 30 samples, 20 had detectable The peanut butter outbreaks have inspired adaptation of new levels of AFB1, ranging from 0.1 to 52.5 ppb (Wang et al., 2001). processing techniques such as electron beam radiation to control pathogens in peanut butter (Hvizdzak, Beamer, Jaczynski, & Matak, 3.2. Peanut butter 2010; Matak, Hvizdzak, Beamer, & Jaczynski, 2010). These technologies need to be further examined for scale-up feasibility and effi- Peanut butter is processed in the same way as peanuts up to the cacy. For example, a study examining high-pressure processing roasting stage, at which time peanuts are finely ground into a paste (HPP; 600 MPa for 5 min at 45 C) against inoculated Salmonella in and vacuum packaged. The standard of identity of peanut butter is peanut butter found only <2 log unit reductions (Grasso, Somerville, similarly defined in the Code of Federal Regulations, which also Balasubramaniam, & Lee, 2010). Since a 6.7 log unit reduction by HPP allows for seasoning and stabilizers (CFR, 2010b). Peanut butter has was achieved in a mixture of peanut flour and water, the fat content 1% moisture and aw of 0.2e0.33 (Burnett, Gehm, Weissinger, & in oil could have provided protection for pathogens. Beuchat, 2000). Thermal treatment of peanut butter may not always be effective Similar to peanuts, Salmonella can survive in peanut butter as well. Typically, Salmonella can be destroyed by heating food to despite its low aw. Burnett et al. (2000) found that with an initial 71 C for a few seconds. Yet, Salmonella has been shown to survive inoculum of 5.68 log CFU/g, Salmonella was found at greater than in peanut butter heated to 90 C(Shachar & Yaron, 2006). A possible 3 log CFU/g after 1 week at 5 C and 21 C. Even after 24 weeks, explanation is that the high fat content provides local buffer regions approximately 2 and 1 log CFU/g Salmonella was detected at 5 C that allow Salmonella to survive with increased heat resistance. and 21 C, respectively. A 3-strain cocktail of Salmonella tennessee Heat shock proteins can be produced by bacteria, allowing them to inoculated in peanut butter survived for 2 weeks at 4 and 22 C survive better in adverse environmental conditions. Furthermore, (Park, Oh, & Kang, 2008). Further, Kenney and Beuchat (2004) re- a study modeling Salmonella thermal inactivation curves showed ported that another pathogen, Listeria monocytogenes could also outbreak strains of S. tennessee to have increased heat resistance survive for 24 weeks in peanut butter at 20 C with an initial compared to strains that caused sporadic cases (Ma et al., 2009). inoculation level of 4 log CFU/g. Although no illness was reported, The minimum time necessary to reduce the outbreak strains by potential contamination by L. monocytogenes also prompted 7 log units at 90 C was approximately double the time required for nationwide recalls of certain brands of peanut butter, and peanut other strains, at 120 min compared to 55e86 min, respectively (Ma butter & jelly sandwiches in 2010 and 2011 respectively (US FDA, et al., 2009). This finding suggests peanut butter and other high fat, 2010; US FDA 2011a). Results of these studies suggest that any low aw foods cannot simply be heated to destroy all potential pathogen that contaminates peanut butter after heat processing Salmonella. Additionally, a sub-lethal heat process that would could remain in the product throughout its shelf life. normally function as a critical kill step under the correct temperature requirements could instead induce new stress response 3.2.1. Salmonella mechanisms in bacteria (Sirsat et al., 2011). Despite being one of the leading causes of foodborne disease in The simplest peanut butter contamination control methods may the US, Salmonella has not been traditionally associated with be GMPs. GMPs address sanitary water use, sanitary facilities, peanut butter (Scallan et al., 2011). The first documented peanut personal hygiene, plant sanitation, proper transportation, and butter outbreak occurred in1996 in Australia caused by S. Mban- traceback. GMPs and other prevention-based food safety programs daka (Scheil, Cameron, Dalton, Murray, & Wilson, 1998). Ten years must be implemented to prevent any initial contamination to the later, the first peanut butter outbreak occurred in the US, and this product. It is possible that the majority of outbreaks can be pre- multistate outbreak of S. tennessee was attributed to moisture from vented by following proper GMPs. A.S. Chang et al. / Food Control 32 (2013) 296e303 301

3.3. Peanut-derived products control programs is of utmost importance. While peanuts are not typically associated with foodborne illness as they have caused very Other peanut products including peanut flour, peanut granules, few documented outbreaks, peanuts are at risk for aflatoxin peanut meal, peanut paste, and peanut protein are used as ingre- contamination. dients. Peanuts in these various forms are used in a variety of food Peanut butter has recently been implicated in large, national products including confectionery, bakery type desserts, savory outbreaks. Questions arise as to what other outbreaks could be snacks, pet food, etc. Each type of food uses a different processing caused by pathogens that have never been associated with specific method, so the control of peanut safety may be specific to each foods. Salmonella, for example, is ubiquitous and has caused operation. outbreaks in a wide range of products from fresh fruits and vege- Peanut as an ingredient must also be considered for food safety tables to chocolate. Yet another question is why only Salmonella has risk due to the occurrence of recent outbreaks. An outbreak of been the cause of peanut related outbreaks. The peanut butter disease associated with a kosher peanut snack imported from Israel outbreaks have inspired adaptation of new processing techniques occurred in 1994. Twenty seven cases of Salmonella agona infection, to control pathogens in peanut butter. Outbreaks also inspire 26 of which were children, were reported in England and Wales. An improved methods of pathogen detection and regulations to outbreak of S. agona was already occurring in Israel at the time. address consumer concerns. For example, in January 2011, the Food Positive samples ranged from 2 to 45 CFU/packet (Killalea et al., Safety Modernization Act (FSMA) was signed into law (Public Law, 1996). 2011). FSMA aims to improve the capacity of the FDA to detect and The largest outbreak related to peanut derived products respond to potential problems and to improve the safety of involved a Georgia peanut manufacturer in 2009. Besides peanut imported food. All large manufacturing and processing facilities butter, they also manufactured roasted peanuts used in snack mixes must register with the FDA and operate under a hazard analysis, and peanut paste used in cookies, crackers, cereal, candy, ice cream, prevention-based food safety program Hazard Analysis & Critical pet treats, and other products. After epidemiological investigations Control Points (HACCP; pronounced/’hæ-sip/). The Act also pointed to a Georgia peanut manufacturer as the source of the includes requirements for mandatory laboratory testing and outbreak, the FDA investigated their plant in January 2009. The FDA increased frequency of inspections (Public Law, 2011). While food observed numerous poor manufacturing practices including the testing and inspections do not ensure safety, there is increased use of unclean equipment, storing raw peanuts next to roasted potential of detecting a problem and implementing corrective peanuts (i.e., finished product), using uncleanable materials on action. equipment, using the same sink for handwashing and cleaning Prevention of outbreaks is best accomplished through cooper- mops, failing to properly sanitize by allowing mold growth, and ation among all individuals within a food operation and with failing to prevent pests from entering the facility. Gaps in ceilings regulators to implement effective GAPs, GMPs, and other allowed drips inside the plant and onto product. Product was stored prevention-based food safety programs. Peanut operations can near cracks in floors and walls that were contaminated with learn from past outbreaks to provide safe products for consumers. Salmonella. While the manufacturer recognized roasting as a critical control point, they did not validate and properly document the oven temperature (US FDA, 2009b). References Perhaps the most egregious mistake by the Georgia manufacturer was disregarding their internal food safety program. The Antony, M., Shukla, Y., & Janardhanan, K. K. (2003). Potential risk of acute hepato- toxicity of kodo poisoning due to exposure to cyclopiazonic acid. Journal of manufacturer sent samples to third party laboratories for micro- Ethnopharmacology, 87,211e214. biological analyses. When the samples were positive for Salmonella, Beyer, K., Morrow, E., Li, X. M., Bardina, L., Bannon, G. A., Burks, A. W., et al. (2001). they resubmitted samples possibly hoping for negative results that Effects of cooking methods on peanut allergenicity. Journal of Allergy and Clin- e would negate the positives. Regardless of results, product was ical Immunology, 107, 1077 1081. Bhat, R., Rai, R. V., & Karim, A. A. (2010). Mycotoxins in food and feed: present status shipped to buyers including institutions with high-risk pop- and future concerns. Comprehensive Reviews in Food Science and Food Safety, 9, ulations. The same incident occurred 12 times over two years 57e81. before the 2009 outbreak. Even after receiving positive Salmonella Bhavanishankar, T. N., & Shantha, T. (2006). Natural Occurrence of Fusarium toxins in peanut, sorghum and maize from Mysore (India). Journal of the Science and results, the manufacturer continued to use equipment that had Food and Agriculture, 40,327e332. processed contaminated peanut paste without first cleaning it (US Bischoff, S. C., & Sellge, G. (2003). Immune mechanisms in food-induced disease. In FDA, 2009b). Amazingly, this manufacturer remained in operation D. D. Metcalfe, H. A. Sampson, & R. A. Simon (Eds.), Food Allergy: Adverse reactions to foods and food additives (3rd ed.) (pp. 14e37). Malden, MA: Black- for years without incident, when any one of these poor well Publishing, Inc. manufacturing practices could have caused an outbreak. Branum, A. M., & Lukacs, S. L. (2008). Food allergy among US children: trends in In order to prevent such large outbreaks in the future, the FDA prevalence and hospitalizations. NCHS Data Brief, 10,1e8. Burdock, G. A., & Flamm, W. G. (2000). Safety assessment of the mycotoxin cyclo- issued a guidance for industry for food operations that use peanut piazonic acid. International Journal of Toxicology, 19,195e218. derived products as ingredients in food. This document lists GMPs Burnett, S. L., Gehm, E. R., Weissinger, W. R., & Beuchat, L. R. (2000). Survival of specific to peanut derived products used as ingredients, with Salmonella in peanut butter and peanut butter spread. Journal of Applied Microbiology, 89,472e477. special considerations for controlling Salmonella. For example, the Centers for Disease Control and Prevention. (2007). Multistate outbreak of Salmo- FDA recommends manufacturers use suppliers that have validated nella serotype tennessee infections associated with peanut butterdUnited processes that reduce Salmonella in the peanut derived ingredient States, 2006e2007. Morbidity and Mortality Weekly Report, 56,521e524. by 5 log units (US FDA, 2009c). Centers for Disease Control and Prevention. (2009). Multistate outbreak of Salmo- nella infections associated with peanut butter and peanut butter-containing productsdUnited States, 2008e2009. Morbidity and Mortality Weekly Report, 4. Conclusions 58,85e90. Christian, K. A., Schlegal, J., Ard, L., Mays, E., Curry, P., & Davis, M. (2007). Outbreak of Salmonella serotype Thompson associated with boiled peanutsdSouth Caro- Prevention of contamination is the best way to prevent food- lina, 2006. In Centers for disease control and prevention, 56th annual epidemic borne disease outbreaks and should be a goal of every food intelligence service conference (pp. 62), Atlanta, GA: Retrieved 08.07.11, from. processor and handler. Peanuts pose a large risk for individuals http://www.cdc.gov/eis/downloads/2007.EIS.Conference.pdf. Chung, S.-Y., Kato, Y., & Champagne, E. T. (2005). Polyphenol oxidase/caffeic acid with peanut allergy and hence, preventing peanut contamination may reduce the allergenic properties of peanut allergens. Journal of the Science of other foods by following GMPs and implementing allergen of Food and Agriculture, 85, 2631e2637. 302 A.S. Chang et al. / Food Control 32 (2013) 296e303

Chung, S.-Y., Yang, W., & Krishnamurthy, K. (2008). Effects of pulsed UV-light on Matak, K. E., Hvizdzak, A. L., Beamer, S., & Jaczynski, J. (2010). Recovery of Salmonella peanut allergens in extracts and liquid peanut butter. Journal of Food Science, 73, enterica serovars typhimurium and tennessee in peanut butter after electron 400e404. beam exposure. Journal of Food Science, 75, M462eM467. Code of Federal Regulations. (2010a). Title 7, Part 996.11. Minimum quality and Mattes, R. D., Kris-Etherton, P. M., & Foster, G. D. (2008). Impact of peanuts and tree handling standards for domestic and imported peanuts marketed in the United nuts on body weight and health weight loss in adults. The Journal of Nutrition, States: Negative aflatoxin content. Washington, D.C: US Food and Drug Admin- 138,1741Se1745S. istration, Office of the Federal Register. Mehan, V. K., & McDonald, D. (1982). Mycotoxin producing fungi in groundnuts- Code of Federal Regulations. (2010b). Title 21, Part 164.150. Tree nut and peanut potential for mycotoxin contamination. In Proceedings of the international products: Peanut butter. Washington, D.C: US Food and Drug Administration, symposium on mycotoxins and phycotoxins (pp. 98e101), 1e3 September 1982. Office of the Federal Register. Vienna, Austria. ConAgra Foods, Inc. (2007, April 5). ConAgra Foods announces the renovation of its Nishie, K., Cole, R. J., & Dorner, J. W. (1987). Toxic effects of cyclopiazonic acid in the peanut butter plant and enhanced food safety measures. Retrieved 08.07.11, from. early phase of pregnancy in mice. Research Communications in Chemical http://media.conagrafoods.com/phoenix.zhtml?c¼202310&p¼irol- Pathology and Pharmacology, 55, 303e315. newsArticle&ID¼1008473&highlight¼. Ogbadu, G. (1980). Influence of gamma-irradiation of aflatoxin B1 production by Dodo, H. W., Konan, K. N., Chen, F. C., Egnin, M., & Viquez, O. M. (2008). Alleviating Aspergillus flavus growing on some Nigerian foodstuffs. Microbios, 27,19e26. peanut allergy using genetic engineering: the silencing of the immunodo- Park, E.-J., Oh, S.-W., & Kang, D.-H. (2008). Fate of Salmonella tennessee in peanut minant allergen Ara h 2 leads to its significant reduction and a decrease in butter at 4 and 22C. Journal of Food Science, 73,M82eM86. peanut allergenicity. Plant Biotechnology, 6,135e145. Parker, W. A., & Melnick, D. (1966). Absence of aflatoxin from refined vegetable oils. Doughtie, R. T. (1947). Sampling of cottonseed, soybeans and peanuts: methods Journal of the American Oil Chemists’ Society, 43, 635e638. used and problems encountered. Journal of the American Oil Chemists’ Society, Plenge-Tellechea, F., Soler, F., & Fernandez-Belda, F. (1997). On the inhibition þ 24,335e340. mechanism of sarcoplasmic or endoplasmic reticulum Ca2 -ATPases by cyclo- Eglezos, S. (2010). The bacteriological quality of retail-level peanut, almond, cashew, piazonic acid. Journal of Biological Chemistry, 272, 2794e2800. hazelnut, Brazil, and mixed nut kernels produced in two Australian nut- Public Law. (2004). Food allergen labeling and consumer protection. Pub L no. 108e processing facilities over a period of 3 years. Foodborne Pathogens and 282, 118 Stat. 905. Disease, 7, 863e866. Public Law. (2011). FDA food safety modernization act. Pub L no. 111e353, 124 Stat El-Maghraby, O. M. O., & El-Maraghy, M. S. S. (1987). Mycoflora and mycotoxins of 3885. peanut (Arachis hypogaea L.) seeds in Egypt. 1-sugar fungi and natural occur- Reese, G., & Lehrer, S. B. (1999). Food allergens. In M. Frieri, & B. Kettelhut (Eds.), rence of mycotoxins. Mycopathologia, 98,165e170. Food hypersensitivity and adverse reactions: a practical guide for diagnosis and Federal Register. (2011). Enhancing airline passenger protections, Vol. 76. Washington, management (pp. 69e97). New York: Marcel Dekker, Inc. D.C: US Department of Transportation, Retrieved 08.07.11, from. http://www. Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M.-A., Roy, S. L., federalregister.gov/articles/2011/04/25/2011-9736/enhancing-airline- et al. (2011). Foodborne illness acquired in the United Statesdmajor pathogens. passenger-protections#h-58. Emerging Infectious Diseases, 17,7e15. Grasso, E. M., Somerville, J. A., Balasubramaniam, V. M., & Lee, K. (2010). Minimal Scheil, W., Cameron, S., Dalton, C., Murray, C., & Wilson, D. (1998). A South effects of high-pressure treatment on Salmonella enterica serovar typhimurium Australian Salmonella Mbandaka outbreak investigation using a database to inoculated into peanut butter and peanut products. Journal of Food Science, 75, select controls. Australian and New Zealand Journal of Public Health, 22, E522eE526. 536e539. Griel, A. E., Eissenstat, B., Juturu, V., Hsieh, G., & Kris-Etherton, P. M. (2004). Scott, P. M. (1998). Industrial and farm detoxification process for mycotoxins. Revue Improved diet quality with peanut consumption. Journal of the American College Med Vet., 149, 543e548. of Nutrition, 23,660e668. Shachar, D., & Yaron, S. (2006). Heat tolerance of Salmonella enterica serovars agona, Gupta, R. S., Springston, E. E., Warrier, M. R., Smith, B., Kumar, R., Pongracic, J., et al. Enteritidis, and typhimurium in peanut butter. Journal of Food Protection, 11, (2011). The prevalence, severity, and distribution and childhood food allergy in 2687e2691. the United States. Pediatrics, 128,e9ee17. Sicherer, S. H., & Sampson, H. A. (2010). Food allergy. Journal of Allergy and Clinical Hourihane, J. O., Bedwani, S. J., Dean, T. P., & Warner, J. O. (1997). Randomised, Immunology, 125,S116eS125. double blind, crossover challenge study of allergenicity of peanut oils in Sirsat, S. A., Burkholder, K. M., Muthaiyan, A., Dowd, S. E., Bhunia, A. K., & Ricke, S. C. subjects allergic to peanuts. British Medical Journal, 314, 1084e1088. (2011). Effect of sublethal heat stress on Salmonella typhimurium virulence. Hvizdzak, A. L., Beamer, S., Jaczynski, J., & Matak, K. E. (2010). Use of electron beam Journal of Applied Microbiology, 110,813e822. radiation for the reduction of Salmonella enterica serovars typhimurium and Staron, T., Thirouin, D., Perrin, L., & Frere, G. (1980). Microwave treatment of bio- tennessee in peanut butter. Journal of Food Protection, 73,353e357. logical food production. Industrie Alimentari Agricole, 12, 1305e1312. International Agency for Research on Cancer. (2002). Some traditional herbal Subrahmanjan, P., & Rao, A. S. (1974). Occurrence of aflatoxins and citrinin in medicines, some mycotoxins, naphthalene and styreneIn IARC monographs on the groundnut (Arachis hypogaea L.) at harvest in relation to pod condition and evaluation of carcinogenic risks to humans, Vol. 82. Lyon, France: IARC, 301e366. kernel moisture content. Current Science, 43,707e710. Kamika, I., & Takoy, L. L. (2011). Natural occurrence of Aflatoxin B1 in peanut Taylor, S. L., Busse, W. W., Sachs, M. I., Parker, J. L., & Yunginger, J. W. (1981). Peanut collected from Kinshasa, Democratic Republic of Congo. Food Control, 22,1760e oil is not allergenic to peanut-sensitive individuals. Journal of Allergy and Clinical 1764. Immunology, 68,372e375. Kenney, S. J., & Beuchat, L. F. (2004). Survival, growth, and thermal resistance of Taylor, S. L., Crevel, R. W. R., Sheffield, D., Kabourek, J., & Baumert, J. (2009). Listeria monocytogenes in products containing peanut and chocolate. Journal of Threshold dose for peanut: risk characterization based upon published results Food Protection, 67, 2205e2211. from challenges of peanut-allergic individuals. Food and Chemical Toxicology, 47, Killalea, D., Ward, L. R., Roberts, D., de Louvois, J., Sufi, F., Stuart, J. M., et al. (1996). 1198e1204. International epidemiological and microbiological study of outbreak of Salmo- Taylor, S. L., & Hefle, S. L. (2005). Allergen control. Food Technology, 59,40e43, 75. nella agona infection from a ready to eat savoury snackdI: England and Wales Urano, T., Trucksess, M. W., Beaver, R. W., Wilson, D. M., Dorner, J. W., & Dowell, F. E. and the United States. British Medical Journal, 313,1105e1107. (1992). Co-occurrence of cyclopiazonic acid and aflatoxins in corn and peanuts. Kirk, M. D., Little, C. L., Lem, M., Fyfe, M., Genobile, D., Tan, A., et al. (2004). An Journal of AOAC International, 75, 838e841. outbreak due to peanuts in their shell caused by Salmonella enterica serotypes US Department of Agriculture. (2010). Food availability (per capita) data system: Stanley and Newportdsharing molecular information to solve international peanuts and tree nuts. Retrieved 08.07.11, from. http://www.ers.usda.gov/Data/ outbreaks. Epidemiology and Infection, 132,571e577. FoodConsumption/Spreadsheets/nuts.xls. Kishore, K. G., Pande, S., Manjula, K., Rao, N. J., & Thomas, D. (2002). Occurrence of US Department of Agriculture. (2011a). Crop production 2010 summary. Retrieved mycotoxins and toxigenic fungi in groundnut (Arachis hypogaea L.) seeds in 08.07.11, from. http://usda.mannlib.cornell.edu/usda/current/CropProdSu/ Andhra Pradesh, India. Plant Pathology Journal, 18,204e209. CropProdSu-01-12-2011_new_format.pdf. Komitopoulou, E., & Penaloza, W. (2009). Fate of Salmonella in dry confectionery US Department of Agriculture. (2011b). Crop values 2010 summary. Retrieved raw materials. Journal of Applied Microbiology, 106, 1892e1900. 08.07.11, from. http://usda.mannlib.cornell.edu/usda/current/CropValuSu/ Kotz, D., Simpson, C. R., & Sheikh, A. (2011). Incidence, prevalence, and trends of CropValuSu-02-16-2011.pdf. general practitioner-recorded diagnosis of peanut allergy in England, 2001 to US Department of Agriculture, Agricultural Marketing Service. (2004). Milled 2005. Journal of Allergy and Clinical Immunology, 127, 623e630. peanuts, inspection Instructions. Washington, D.C: U.S. Gov. Print Office, Lansden, J. A., & Davidson, J. I. (1983). Occurrence of cyclopiazonic acid in peanuts. Retrieved 07.11.2, from. http://www.ams.usda.gov/AMSv1.0/getfile? Applied and Environmental Microbiology, 45,766e769. dDocName¼STELPRDC5098115. Lee, S., Oh, S., Jang, D., Lee, J., & Byun, M. (2008). Evaluation of reduced allergenicity US Food and Drug Administration. (2000). Guidance for industry: action levels for of peanut extract by gamma irradiation in murine model of peanut allergy. poisonous or deleterious substances in human food and animal feed. Retrieved 08.07.11, Journal of Allergy and Clinical Immunology, 121, S184. from. http://www.fda.gov/Food/GuidanceComplianceRegulatoryInformation/ Ma, L., Zhang, G., Gerner-Smidt, P., Mantripragada, V., Ezeoke, I., & Doyle, M. P. GuidanceDocuments/ChemicalContaminantsandPesticides/ucm077969.htm. (2009). Thermal inactivation of Salmonella in peanut butter. Journal of Food US Food and Drug Administration. (2009a). FDA’s investigation. Retrieved 08.07.11, Protection, 72, 1590e1601. from. http://www.fda.gov/Safety/Recalls/MajorProductRecalls/Peanut/FDA%E2% Magnoli, C., Astoreca, A., Ponsone, M. L., Fernández-Juri, M. G., Barberis, C., & 80%99sInvestigation/default.htm. Dalcero, A. M. (2007). Ochratoxin and Aspergillus section Nigri in peanut seeds US Food and Drug Administration. (2009b). Redacted amended FDA 483 for PCA. in different months of storage in Córdoba, Argentina. International Journal of Retrieved 08.07.11, from. www.fda.gov/downloads/AboutFDA/CentersOffices/ Food Microbiology, 119,213e218. ORA/ORAElectronicReadingRoom/UCM109834.pdf. A.S. Chang et al. / Food Control 32 (2013) 296e303 303

US Food and Drug Administration. (2009c). Guidance for industry: Measures to Vierk, K., Falci, K., Wolyniak, C., & Klontz, K. C. (2002). Recalls of foods containing address the risk for contamination by Salmonella species in food containing undeclared allergens reported to the US Food and Drug Administration, fiscal a peanut-derived product as an ingredient. Retrieved 08.07.11, from. http://www. year 1999. Journal of Allergy and Clinical Immunology, 109, 1022e1026. fda.gov/Food/GuidanceComplianceRegulatoryInformation/ Wang, J.-S., Huang, T., Su, J., Liang, F., Wei, Z., Liang, Y., et al. (2001). Hepatocellular GuidanceDocuments/ProduceandPlanProducts/ucm115386.htm. carcinoma and aflatoxin exposure in Zhuqing Village, Fusui county, People’s US Food and Drug Administration. (2010). Recalls, market withdrawals & safety Republic of China. Cancer Epidemiology, Biomarkers & Prevention, 10,143e146. alerts. Retrieved 27.05.12 from. http://fda.gov/Safety/Recalls/ucm197823.htm. Whitaker, T. B., & Dowell, F. E. (1995). Sampling methods to measure aflatoxin and US Food and Drug Administration. (2011a). Recalls, market withdrawals, & safety grade factors of peanuts. In H. E. Pattee, & H. T. Stalker (Eds.), Advances in peanut alerts. Retrieved 2705.12 from. http://fda.gov/Safety/Recalls/ucm247000.htm. science (pp. 475e499). American Peanut Research and Education Society, Inc. US Food and Drug Administration. (2011b). Recalls, market withdrawals, & safety Whitaker, T. B., Springer, J., Defize, P. R., DeKoe, W. J., & Coker, R. (1995). Evaluation alerts. Retrieved 08.07.11, from. http://www.fda.gov/Safety/Recalls/ of sampling plans used in the United States, United Kingdom, and the ucm245897.htm. Netherlands to test raw shelled peanuts for aflatoxin. Journal of AOAC Interna- Van Egmond, H. P. (1989). Current Situation on regulations for mycotoxins. Over- tional, 78,1010e1018. view of tolerances and status of standard methods of sampling and analysis. Wild, C. P., & Gong, Y. Y. (2010). Mycotoxins and human disease: a largely ignored Food Additives and Contaminants, 6,139e188. global health issue. Carcinogenesis, 31,71e82. Van Rensburg, S. J. (1984). Subacute toxicity of the mycotoxin cyclopiazonic acid. Woodroof, J. G. (Ed.), (1983). Peanuts: production, processing, products (3rd ed.). Food and Chemical Toxicology, 22, 993e998. Westport, CN: The Avi Publishing Company, Inc.