Improving the safety of almonds and pistachios

15 Improving the safety of almonds and pistachios L. J. Harris and L. Ferguson, University of California, Davis, USA DOI: 10.1533/9780857097484.2.350 Abstract: This chapter discusses microbiological safety of almonds and pistachios. An overview of the basic production or growing practices is provided along with general post-harvest handling and processing schemes that compare and contrast the two nuts. Sources and routes of contamination of these nuts with foodborne pathogens and mycotoxigenic molds is covered in addition to some of the pre- and post-harvest practices that may be used to minimize the potential for contamination. Factors affecting survival and growth in the production and processing environments, and processing methods used to reduce microbial loads are discussed. Keywords: almond, Prunus dulcis, pistachio, Pistacia vera, tree nut, foodborne.

15.1

Introduction and historical perspective

Although classified as nuts in commercial horticulture and for culinary purposes, both almonds (Prunus dulcis) and pistachios (Pistacia vera) are classified botanically as drupes. A drupe is an indehiscent fruit in which the fertilized embryo (seed or kernel) within a hardened endocarp (shell) is surrounded by a fleshy mesocarp (hull) and an exocarp (external skin). In most other tree fruits classified as drupes, such as apricots, peaches, plums and cherries, the combined mesocarp and exocarp (hull and skin) are the edible fruits. In almonds and pistachios the kernel is the commercial edible product for human consumption; dried almond hulls are used for animal feed and pistachio hulls are generally spread onto fallow fields. The current cultivated almond is thought to originate from wild species of Amygdalus communis that grew in central and southwest Asia (Kester and Ross, 1996). The tree was well adapted to mild, wet winters and dry, hot summers. The wild plants yielded predominantly bitter seeds due to the presence of the glycoside

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amygdalin. Cultivation of progressively sweeter kernels selected from the wild varieties is thought to have occurred thousands of years ago. Cultivation spread from Asia to the Middle East and ultimately to the Mediterranean region. Almonds may have been popular to cultivate, in part, because they are adapted to drought and poor soils and traditionally were grown on marginal soils without irrigation. Almonds were first cultivated in the eastern United States by early colonists, but in the 1800s the trees were observed to thrive in the Central Valley of California, which is known for its Mediterranean-like climate. Today, California leads world almond production with estimates of 60 to 80% of the total production on over 6000 farms in the state (ABC, 2012). Australia ranks second, followed by Spain and modest production in other countries on the Mediterranean coast (Greece, Italy, Algeria, Morocco, Syria, Tunisia, and Turkey), Iran and China. Approximately 30 major commercial varieties of almonds are grown in California, and 10 major varieties account for most of the production (ABC, 2012). Two or more almond varieties with complementary pollen shedding and bloom periods are typically planted in alternating rows in an orchard to facilitate the cross pollination necessary for good nut formation. The trees bloom in February; managed honey bee populations are used to transfer pollen between almond trees of different varieties that are pollen compatible. Almonds are harvested from July through November, depending on the variety. Almond trees are deciduous, losing their leaves shortly after harvest. Some almond varieties have a hard shell that requires physical force to remove, whereas others have a paper shell that is easily removed by hand. Paper-shell varieties make up more than 50% of the plantings in California. The pistachio tree originates from Iran and Iraq. Iran leads the world in production but the US has seen significant recent plantings in the states of California and Arizona in the latter part of the 20th and first part of the 21st century. Other major producers include Turkey, Syria and China. In the US, the first commercial harvest of pistachios took place in 1976 (CDPR, 2003). Today, pistachios are grown commercially in the southwestern states of California, Arizona and New Mexico, although over 98% of the industry is located in California’s southern Central Valley. Both the nut-bearing scions and the rootstocks are species within the genus Pistacia. The inedible Pistacia integerrima and atlantica species and their hybrids are used for the rootstocks, and were selected based on resistance or tolerance to the soil-borne fungus Verticillium dahliae. Pistachios are dioecious, with both female trees (fruit-bearing) and male trees (pollinizers). The only edible Pistacia species is P. vera. Female trees of this species grown in the US are primarily cv. Kerman, although two new cultivars (Golden Hills and Lost Hills) have recently been introduced. The pollinizer male trees (cv. Peters and Randy) are uniformly distributed among the compatible female trees at a ratio of about one male to 19–24 female trees (Beede et al., 2008). The apetalous female flowers lack nectaries and do not attract insects, so they are wind pollinated. In general, pistachios are harvested from mid-September to mid-October, with most of the harvest completed within three weeks. With the new cultivars, Lost Hills and Golden Hills, and their pollinizer, cv. Randy, the

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very brief mid-April bloom has been slightly extended to two weeks and the September to October harvest has been slightly extended to six weeks. Almonds are eaten out-of-hand as plain, roasted and, sometimes, flavored kernels, with the brown skin intact. They are also used in a wide variety of food products from cereals to snack foods and confectionary products. Various forms of almonds are sold, including blanched, diced, sliced, slivered and chopped as well as pastes, butters and flours and these forms can be incorporated into savory as well as sweet products. Pistachios are often roasted and salted or flavored and eaten out-of-hand as in-shell kernels. The shells, when split, are easily removed by hand, and a significant portion of the crop is sold in-the-shell. The shell is naturally a light cream color and the kernel a distinctive green. At one time pistachios were dyed red to cover shell staining caused by delays between harvest and hulling, but this practice is rarely done today. Like almonds, pistachios also may be sold as ingredients (as kernels, pieces, flour and paste) for a wide variety of savory or sweet products.

15.2

Production, harvest and post-harvest practices

Almonds are harvested beginning about 3 years after the tree is planted (Duncan et al., 2011). Almond harvest occurs after the kernels have reached maturation and the hulls begin to split and dry (Fig. 15.1). Once the hull splits, the shell is exposed. Kernels are protected by the shell to varying degrees; kernels may be visible, especially along the suture in paper-shell varieties. Traditionally, almonds were hand knocked to the ground using poles, sometimes onto tarps, and left to dry. In the first harvest year, the trees are small and the almonds may still be hand harvested at this stage. However, most almond trees older than 3 years are mechanically harvested except in very small orchards with few trees or in terrain where mechanical shakers cannot access the trees. Equipment used to shake the trees causes the almonds to drop to the orchard floor; drying times on the ground depend on the initial moisture content of the nuts, and may vary from 1 to 2 weeks for earlyharvested crop, or 4 to 7 days for later-harvested crop in which drying may have begun on the trees (Reil et al., 1996). Optimal hull moisture of 8 to 12% ensures efficient hulling (Thompson et al., 1996). Target water activity for stored almonds is below 0.65 water activity (approximately 6% moisture) (Kader, 1996). This level of water activity eliminates growth of bacteria and fungi, including Aspergillus flavus and Aspergillus parasiticus, which can produce aflatoxin (see Section 15.5). Although relatively uncommon, rain may fall, especially during the latter harvest months, resulting in various degrees of rehydration of almonds on the ground. In addition, some almonds may prematurely drop from the trees and become soaked with irrigation water. Almonds are moved about on the orchard floor by harvesting equipment and are mixed repeatedly, which increases the points of contact with the orchard floor and other nuts. The harvested almonds are also in the direct path of significant dusts generated by the shaker-harvesters and windrowing and collecting machines.

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Fig. 15.1

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Flow diagram showing general steps in harvesting and processing almonds.

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After the drying period, the almonds are swept from around the trees and piled into windrows between the rows of trees. The windrows are mechanically collected from the orchard floor while pressurized air is used to remove light debris. Almonds may be temporarily stored in stockpiles on the farm or after being transported to hulling/shelling facilities. Stockpiles are sometimes covered with tarps for fumigation with insecticides, such as phosphine, to control insect damage (Kader and Thompson, 1992). Tarped and fumigated almonds may be stored for several months prior to hulling. Almond huller-sheller facilities are most often completely separate from the processing facilities. In the first step, leaves, sticks, stones and soil are mechanically removed. Some almonds are hulled but not shelled; however, most are both hulled and shelled simultaneously in a series of shear rollers (Thompson et al., 1996). The kernels may be further cleaned and sorted for quality and size either at the huller-sheller, or more commonly after arrival at the processor (handler). Kernels may be stored in bins or in silos, often at ambient temperature. The high soluble-sugar content of almond hulls makes them an excellent nutrient source for animals, and the majority of the hulls produced in California are sold for dairy cattle feed (Aguilar et al., 1984). Shells are sold primarily for use as livestock bedding, artificial fire logs or other energy sources. Although the ratios vary with variety, each kilogram of kernels produces approximately 2 kg of hulls and 0.5 kg of shells. Pistachios develop in large clusters on the tree. In California, the nuts are shaken directly into a catch frame, so they do not come in contact with the orchard floor (Fig. 15.2). They are conveyed into bins or trailers for transport to the hulling facility. The shells of most of the pistachios will have naturally split at the time of harvest, but the fleshy hulls typically remain intact. To avoid staining of the shells, pistachios are ideally hulled within a few hours of harvest at facilities that are usually collocated with processing facilities. After pre-cleaning to remove leaves, sticks and other debris, hulls are removed by abrasion and washed away with water. Kernels that are underdeveloped (less than 50% of shell volume) and insect (especially navel orangeworm) or otherwise damaged and shells with adhering hull can be separated from fully-developed kernels in a tank of water (float tank) because the most desirable nuts sink. Thereafter, the ‘sinker’ (85 to 90% of the crop) and ‘floater’ (10 to 15% of the crop) streams are handled separately. The proportion of sinkers to floaters varies with year and harvest conditions. The product passes through a continuous dryer for up to 24 h at initial temperatures of approximately 80 to 105°C and final temperatures of about 70°C. The nuts are dried to moisture levels of 8 to 15% and then moved to large silos. Ambient air is introduced into the silos for several days until the nuts have equilibrated to moisture levels of 5 to 7%. The nuts may be stored in these silos for up to 14 months and are removed as needed for processing. In the US, pistachios are most often sold as a roasted and flavored in-shell snack; the kernel makes up approximately 50% of the weight. Naturally-opened shells are more valuable than artificially split closed-shell sinkers. Closed-shell sinkers may also be cracked to produce whole kernels or pieces. The floater stream is shelled and sorted. Fully-

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Fig. 15.2

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Flow diagram showing general steps in harvesting and processing pistachios.

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mature kernels may be blended with the sinker stream kernels; others are sold as animal feed.

15.3

Microbiological safety

15.3.1 Outbreaks and recalls linked to Salmonella Four reported outbreaks of salmonellosis have been associated with consumption of raw almonds (Table 15.1); no reported outbreaks of foodborne illness have been associated with consumption of pistachios. The first almond outbreak was identified in Canada and ultimately linked to the consumption of raw California almond kernels that were sold in bulk (Isaacs et al., 2005). A total of 157 cases from five provinces were reported from December of 2000 through July 2001, with peaks in cases occurring in mid-December and mid-April. The outbreak was identified, in part, because at that time the investigators in Ontario, Canada, routinely determined the phage type of isolates of Salmonella Enteritidis. In doing so, clusters of phage type 30 (PT 30) isolates, a rare type previously unknown in the US and Canada, were identified, ultimately leading to the outbreak investigation. Previously, Salmonella Enteritidis PT 30 had only been isolated in other countries from a variety of poultry-related products (Chart et al., 1991). The outbreak strain was isolated from unopened boxes of bulk raw almonds from four implicated lots at a prevalence of about 65% (Danyluk et al., 2006; Isaacs et al., 2005). Traceback investigations eventually led to a processor, then a huller-sheller, and ultimately a group of orchards. The outbreak strain was also isolated from swabs of equipment surfaces at both the processor and huller-sheller and from swabs of the floors of the almond orchards 6 to 9 months after the outbreak-associated almonds were harvested. The second outbreak was identified in 2004 and linked to product harvested in 2003 (CDC, 2004; CDPH, 2004). The PFGE fingerprint of the outbreak strain was Table 15.1 Outbreaks of salmonellosis associated with the consumption of raw whole almonds Salmonella serovar

Isolated from product?

Year

Confirmed cases (no.)

Outbreak location(s)

Typhimurium

Yes

2012

27

Australia

Enteritidis

No

2005–2006

15

Enteritidis PT 9c

No

2004

47

2000–2001

168

Enteritidis PT 30 Yes

Reference

Whitworth, 2012 Sweden Ledet Müller et al., 2007 Canada, USA CDC, 2004; CDPH, 2004 Canada, USA CDPH, 2002; Chan et al., 2002; Isaacs et al., 2005

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very similar to the 2001 strain, leading to inclusion of raw almonds in the preliminary case/control questionnaire. Salmonella Enteritidis PT 9c, another rare phage type, was linked to this outbreak. This strain was later shown to be highly genetically related to the 2001 outbreak strain (Parker et al., 2010). The third raw almond outbreak occurred in Sweden in 2005 and 2006 and was again linked to Salmonella Enteritidis PT 30 (Ledet Müller et al., 2007). In 2012, an Australian outbreak of salmonellosis was associated with consumption of raw almonds grown in that country (Whitworth, 2012). Salmonella Typhimurium was isolated from a total of 27 confirmed cases and from the implicated almonds. Pistachios have not been linked to a foodborne outbreak; a large recall of pistachios and pistachio-containing products was initiated in March 2009 when Salmonella Montevideo was identified in the roasted pistachios that were used as an ingredient in a trail mix (FDA, 2009). 15.3.2 Prevalence and concentration of enteric pathogens In recalled lots of raw almonds from the 2000 to 2001 outbreak, 65% of 100 g samples tested were positive for the outbreak strain (Table 15.2) (Danyluk et al., 2007). Salmonella population levels of <0.3 most probable number (MPN) per gram were reported upon initial testing in July 2001; later testing in August 2001 using larger sample sizes revealed very low but measurable levels of Salmonella (6 to 9 MPN/100 g) (Danyluk et al., 2007). Back calculation using predicted population reductions indicated that levels of Salmonella in the almonds in February at the time of the outbreak peak might have been in the range of one to several hundred per 100 g (Danyluk et al., 2007; Lambertini et al., 2012). Subsequent to the outbreak, the almond industry in California sponsored a multi-year survey to evaluate the prevalence of Salmonella in raw almonds collected from around the state shortly after harvest. Based on the outbreak data 100g samples were evaluated, rather than the standard 25 g used in many routine prevalence surveys. Roughly 2000 samples per year (total 13 972) were evaluated over a total of eight years (Table 15.2) (Bansal et al., 2010; Danyluk et al., 2007; Lambertini et al., 2012). The Salmonella prevalence ranged from 0.6 to 1.6% with an average of 1% (Lambertini et al., 2012). The levels of Salmonella in 99 positive samples from five out of eight years were determined using a three-tube MPN technique with 25, 2.5 and 0.25g samples sizes. In most cases Salmonella was not isolated during the MPN analysis (Bansal et al., 2010; Danyluk et al., 2007); calculated levels of the organism in positive samples was at least an order of magnitude lower than levels predicted for the 2001 outbreak, ranging from 4 MPN/1000 g (most samples) to 150 MPN/1000 g (one sample). The California pistachio industry also funded Salmonella prevalence surveys for raw pistachios collected from storage silos shortly after harvest. Prevalence of Salmonella in 100g in-shell pistachio samples in 2010 and 2011 was 0.95% (11 of 1152) and 0.43% (six of 1380), respectively (Lieberman and Harris, unpublished). Levels of Salmonella in the positive samples were in line with those measured for

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Table 15.2

Prevalence and concentration of Salmonella in California raw almonds

Nut, form

Harvest year

No. of positive 100 g samples

% positive

Range Reference (MPN/1000 g)

Almond, kernel

2000*

32 out of 50

64

61–91

2001†

12 out of 2003

0.60

ND

2002

24 out of 2012

1.2

7.9–32

2003

15 out of 1764

0.85

7.9–19

2004

12 out of 1643

0.73

7.9–19

2005

18 out of 1852

0.97

4.4–22

2006

31 out of 1899

1.6

7.9–50

2007

15 out of 1799

0.83

ND

2010

10 out of 1000

1.0

ND

2006

2 out of 229

0.87

ND

2007

5 out of 226

2.2

ND

Almond, in-shell

Danyluk et al., 2006 Danyluk et al., 2007 Danyluk et al., 2007 Danyluk et al., 2007 Danyluk et al., 2007 Danyluk et al., 2007 Bansal et al., 2010 Bansal et al., 2010 Harris, unpublished Bansal et al., 2010 Bansal et al., 2010

* Almonds recalled from 2000–2001 outbreak; % positive and MPN performed July 2001 for almonds harvested in fall of 2000. † Almond Board of California survey data; random samples of almonds arriving at processing facilities throughout California.

ND, not determined.

almonds and ranged from 5 MPN/1000 g (most samples) to 72 MPN/1000 g (one sample). There have been several retail-based surveys for tree nuts in the United Kingdom (Table 15.3) and one processor survey in Australia (Eglezos et al., 2008). All of these surveys have used the standard 25g sample for analysis, making it more challenging to recover very low levels of Salmonella expected in these products. Nevertheless, one of 60 raw almond samples collected at an Australian processor was positive for Salmonella Fremantle (Eglezos et al., 2008) and one of four samples of roasted pistachios collected at retail was positive for Salmonella Havana (Little et al., 2009). With most retail surveys, it is challenging to know the country of origin, distribution, processing and age of the product being tested. Rather, they offer a snapshot of products available to the consumer over a given period of time. The number of samples collected (2 to 359) for each nut type is also typically insufficient to determine prevalence rates when those rates are anticipated to be 1% or less.

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Surveys of almonds and pistachios for Salmonella in 25g samples

Nut

Almond Raw kernels Treated (roasted and unknown) Roasted kernels Treated Various packaged and unpackaged nut products Pistachio Raw whole Kernels only (73), with shells (111) Roasted kernels Various packaged and unpackaged nut products

Where collected No. positive Salmonella for Salmonella/ serovar no. of samples tested

References

Processor receiving, Australia Retail, UK

1/60

Eglezos et al., 2008

0/359

1 Fremantle subsp. II 0

Retail, UK RTE packages at processor, Australia Retail, manufacturers, and growers, Australia

0/83 0/42

0 0

Little et al., 2009 Eglezos, 2010

0/131

0

NSW Food Authority, 2012

Retail, Scotland 0/2

0

Retail, UK

0/184

0

Candlish et al., 2001 Little et al., 2010

Retail, UK Retail, manufacturers, and growers, Australia

1/25 0/76

Havana 0

Little et al., 2010

Little et al., 2009 NSW Food Authority

15.3.3 Factors affecting survival and growth of enteric pathogens Available data on the fate of enteric pathogens in almonds and pistachios are in line with data on other low-moisture foods including pecans and walnuts (Beuchat and Mann, 2010; Blessington et al., 2012). Generic E. coli, E. coli O157:H7, Listeria monocytogenes and Salmonella inoculated onto almonds or pistachios can be recovered for months to years (Kimber et al., 2012; King and Jones, 2001; King et al., 1970; Kokal, 1965; Kotzekidou, 1998; Uesugi et al., 2006). Relative reductions of the pathogens are similar for almonds and pistachios (Fig. 15.3). Survival improves as the storage temperature decreases with little to no reduction at 4°C or below. At 24°C, population levels of E. coli O157:H7 and L. monocytogenes fell more quickly than Salmonella over the first 100 days of storage but distinct tailing of the populations was observed (Kimber et al., 2012). Lambertini et al. (2012) analyzed data from seven 23°C storage studies with Salmonella Enteritidis PT 30-inoculated almonds and one study with six-strain Salmonella cocktail-inoculated almonds; linear rates of reduction ranged from 0.16 to 0.32 log CFU/month (median 0.24 log CFU/month). Although the

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Fig. 15.3 Survival of L. monocytogenes (a), Salmonella (b), or E. coli O157:H7 (c) on the surface of inoculated almonds (squares) or pistachios (circles) stored at 4°C (closed symbols) or 23°C (open symbols) for up to 21 months (630 days). Non-selective media. n/6 indicates that n of 6 samples were below the limit of detection (log 0.3 CFU/g). Adapted from Kimber et al., 2012.

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calculated linear rates of reduction were significant in some of the four −18°C storage studies, they also were very low: 0.02 to 0.05 log CFU/month or approximately 1-log CFU/g reduction in 50 to 20 months, respectively. Significantly better survival of Salmonella on almonds was observed when the inoculum was collected from culture prepared as a lawn on a petri dish compared to the more standard broth preparation (Uesugi et al., 2006). Keller et al. (2012) made the same observation in inoculated peanut butter. Uesugi and Harris (2006) also showed that the longer Salmonella was incubated in a wet solution of almond hulls the more desiccation tolerant the organism was when the hulls were dried. The practical implications of these findings are not known; however, for studies evaluating the survival of Salmonella during desiccation or during long-term storage of dried products, researchers should consider methods used to prepare the inoculum as a significant contributing factor.

15.4

Sources and routes of contamination with enteric pathogens

Almonds and pistachio kernels are assumed to be sterile when on the tree and enclosed in an intact hull. Microbial contamination is assumed to occur after the kernel is exposed either on the tree (some almonds after hull split) or after harvest. In 1966, Kokal and Thorpe (1969) studied the occurrence of E. coli in Nonpareil almonds (a paper-shell variety) from a single orchard in California. E. coli was found among mature almonds taken either from the trees or after shaking to the ground. The levels of occurrence of E. coli increased dramatically starting from the point where the almonds were swept up during collection and throughout the pre-hulling and hulling procedures. After the shells were removed, E. coli incidence dropped from 40% to a final level of 4 to 8% in the raw kernels. The amount of soil mixed with harvested almonds influences the total aerobic plate counts of the kernels (King et al., 1970); samples without visible soil contamination had significantly lower aerobic plate counts than those observed to have attached ‘mud balls’. Mud balls are more likely to be present if the orchard soils are wet during harvest. These observations support the assumption that almonds are vulnerable to contamination during harvest. Almond orchards that were associated with the 2001 outbreak were periodically sampled for Salmonella Enteritidis PT 30 for a period of six years (Isaacs et al., 2005; Uesugi et al., 2007); studies did not extend beyond that period. Two variants of Salmonella Enteritidis PT 30 were isolated on multiple occasions over the sixyear period; this was the only Salmonella isolated from the orchard during that time. Although an eight-year survey excluded almonds from the outbreak orchard, Salmonella Enteritidis PT 30 was isolated from one sample in 2003 (Danyluk et al., 2007) and four samples in 2006 (Bansal et al., 2010) suggesting that the organism might be present in other almond orchards. However, of the 151 Salmonella isolates recovered from almonds, a total of 48 different serovars was identified (Bansal et al., 2010; Danyluk et al., 2007), and eight different serovars were identified from the 17 isolates recovered from pistachios (Harris,

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unpublished). The range of serovars identified was similar to other environmental surveys in California (Gorski et al., 2011; Kinde et al., 1997) suggestive of random environmental contamination of these nuts. Salmonella Enteritidis PT 30 grows in wet almond hull and shell slurries (Uesugi and Harris, 2006), in wetted hulls (Danyluk et al., 2008a), and in wetted dusts that are prevalent in the almond production and hulling environments (Du et al., 2010b). Salmonella can migrate through dry but visually-intact hulls and shells (Danyluk et al., 2008a). When hull extract is added to soil, multiplication of Salmonella can also be demonstrated (Danyluk et al., 2008b). Collectively these data suggest that Salmonella survives in the pre-harvest production environment and, under some circumstances, may be able to multiply in the orchard either in wetted hulls or soils in the absence of an animal host. Almonds come into direct contact with the ground and are efficiently mixed with the top layer of orchard soil during windrowing, pick-up and the hulling and shelling process. The dusts generated during harvest also serve to spread contamination around the orchard and throughout the harvested crop. The trend to planting soft-shell varieties, which have shells that are thin and often open allowing for exposure of the kernel, provides an additional potential for contamination. In addition to direct contamination in the field, kernels may be contaminated during the hulling and shelling process. In most facilities the hulls and the shells are removed at the same time, resulting in considerable mixing of the kernels with both hulls and shells. The hulling and shelling process generates large volumes of dust that can also contribute to contamination of exposed kernels (Du et al., 2007, 2010b; Kokal and Thorpe, 1969). Pistachios are harvested into a catch frame and do not touch the ground. The kernel is encased in the intact fleshy hull, reducing the potential for pre-harvest contamination of the kernel. However, the nuts do mix with leaves and other debris present in the trees. Increases in microbial populations including Salmonella have been shown to occur on in-hull pistachios (Leiberman and Harris, unpublished) when holding times from harvest to hulling exceed the typically less than 4-h period. Hulls are removed by a combination of abrasion and water rinse and then they pass through a water bath (float tank) to separate the product. The float tank provides an opportunity for cross contamination of the hulled product (Kimber and Harris, unpublished). Hulled pistachios are relatively high in moisture (30 to 50%) and reductions in microbial populations (aerobic plate count and coliform count) during drying can be 2 to 3 log CFU/g (Theofel and Harris, unpublished). There is potential for contamination to occur during open transfer of pistachios from the dryer to the silo and as ambient air is forced into the silo for one to three days as the silo is filled and nut moistures equilibrate.

15.5

Aflatoxin

Aflatoxins are secondary metabolites produced by multiple species within the fungal genus Aspergillus (Pier and Richard, 1992). The most toxic aflatoxins are

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produced by A. flavus Link and A. parasiticus Speare; aflatoxin B1 is a potential human liver carcinogen. Most nations have long had regulations concerning the amount of aflatoxin allowed in food and feed products. The US limit for aflatoxin is 20 ppb in all foods; the European Union limits for aflatoxin in ready-to-eat almonds and pistachios are 10 and 8 ppb for total and aflatoxin B1, respectively, and limits for product destined for further processing are 15 and 12 ppb for total and aflatoxin B1, respectively. Molds in the genus Aspergillus have been demonstrated to be present in almonds and pistachios; soil, previously infested nuts and navel orangeworm (Amyelois transitella) are primary reservoirs. The presence of these molds can lead to preharvest decay along with the production of aflatoxin (Campbell et al., 2003; Whitaker et al., 2010). Almond stockpiles must be well managed and condensation minimized with the correct use of tarps to avoid nut moisture increasing to levels that are high enough to support growth of Aspergillus. Navel orangeworm is a moth that infests both almonds and pistachios. Maturing larvae and their feces, called frass, cause damage to the kernels that leads to infection with both A. flavus and A. parasiticus. Pistachios with split and tattered hulls found at the end of harvest also have been demonstrated to have higher levels of aflatoxin as tissues were subject to navel orangeworm infestation (Sommer et al., 1986). As pistachio nuts mature, the shell splits naturally within the fleshy hull. The hull generally remains intact and protects the newly exposed nut surface from invasion by insects, molds and pathogens. However, in 1 to 4% of the nuts the hull adheres to the nut shell and when the shell splits, the hull also splits, thereby exposing the kernel to navel orangeworm and potential contamination with Aspergillus (Doster and Michailides, 1994a, 1994b). For this reason these ‘early splits’ tend to have higher levels of aflatoxin (Sommer et al., 1976); later studies by Doster and Michailides (1994b) found Aspergillus in early splits from most orchards. Until recently, the best method for control of Aspergillus infestations and the resulting aflatoxins was to directly control the naval orangeworm, which is damaging in its own right as well as exacerbating the potential for Aspergillus species. The potential for overwintering of the navel orangeworm is reduced through postharvest orchard sanitation. Orchard sanitation includes knocking ‘mummies’ (unharvested nuts) from the trees before budswell (early February), blowing them to the center of the row and then shredding or otherwise destroying (Duncan et al., 2011). Harvesting soon after the nuts mature also reduces the opportunity for the navel orangeworm to lay eggs. Applying integrated management strategies reduces the need for in-season insecticide application. However, now another more direct method of controlling the toxin producing Aspergillus flavus is available. In early 2012 Aspergillus flavus 36, or AF36, a nontoxic aspergillus was registered in the western pistachio-producing states of California, Arizona, Texas and New Mexico. It limits the development of the aflatoxin producing Aspergillus flavus by out-competing the toxic strain.

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Control consists of spreading SF36, colonized on sterile wheat seeds, over the orchard floor in early summer before the high temperatures that enhance its proliferation. Postharvest approaches to aflatoxin control include removal of insect and other damaged nuts from the product stream by electronic and manual sorting methods. Early-split pistachios tend to have shell staining or discoloration that allows them to be removed by sorting. Both the almond and pistachio industries also have extensive aflatoxin testing programs.

15.6

Good Agricultural Practices (GAPs) to minimize pre-harvest contamination

Good Agricultural Practices (GAPs) for tree nuts overall are discussed in a separate chapter (Chapter 1). GAP programs for tree nuts can be divided into eight general categories: documentation, employee training, nutritional and application practices, water quality, field sanitation and worker hygiene, orchard floor management, pest control, and harvest and delivery sanitation. Commodityspecific GAPs documents are available online for both almonds (ABC, 2009) and pistachios (CPRB, 2009) and up-to-date versions of these documents should be consulted for more information. These general guidelines must be supplemented with specific information from local state and federal regulatory agencies, such as the Pesticide Safety Information Series (PSIS) leaflets available online from the California Department of Pesticide Regulation (CDPR, 2003), and additional information, such as the material safety data sheets (MSDS), available from multiple online sources and from commercial chemical labels. Tree nuts are considered produce for the purposes of the Produce Safety Rule, part of the US Food Safety Modernization Act (FDA, 2013a). At the time this chapter was written the rule was proposed and the comment period was still open. The Produce Safety Alliance (PSA) at Cornell University will ultimately provide materials for standardized training for the produce industry once the rule is published in its final form (PSA, 2013). The California almond and pistachio industries have also produced online GAP materials and self-assessment guidelines (ABC, 2009; CPRB, 2009), which are likely to be updated as the final rule is published. The following summarizes some of the practices recommended to growers by almond and pistachio commodity boards with an emphasis on practices that address the unique aspects of almond and pistachio production. 15.6.1 Documentation and tracking The primary objective of documentation is to be able to track all aspects of nut production. Growers should be able to identify where a specific lot was harvested, the environmental conditions during crop production, all orchard operations, and how the crop was transported and processed.

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Almond and pistachio growers are paid by a combination of the weight and quality of incoming loads of nuts. However, once almonds are hulled, shelled and graded, lots from several orchards or growers may be mixed. Pistachios are similarly mixed in large silos once the hulls and shells have been removed and the nuts dried. While growers may maintain detailed records and documents of production practices, traceback investigations from a finished product may only be possible to a group of orchards harvested on a specific day. 15.6.2 Employee training Because of the high degree of mechanization in the almond and pistachio industries there are few points of direct contact between the worker and the nuts before or during harvest. Crews sometimes prune trees by hand or enter the orchard to remove mummy nuts after harvest. Regardless, employees should attend regularly scheduled training sessions that are updated as needed; training should be documented and evaluated to determine if the programs are effective. The training should include information on the GAP program, the importance of maintaining the integrity of the orchard floor (for almonds), and specific training in the use of portable toilets and hand-washing stations and the appropriate disposal of garbage. Employees should be trained in how to report injury or illness in themselves and fellow employees. 15.6.3 Fertilization and soil amendments Fertilization and soil amendment practices have the potential to introduce enteric pathogens into the orchard. Almonds are particularly at risk during harvesting because they are shaken off trees and remain on the ground to dry, in contact with the soil. Even when harvested onto catch frames, dusts generated in pistachio orchards during harvest potentially contaminate equipment and the crop. Guidelines to avoid contamination from fertilization or soil amendment practices are generally the same. Manure may be used in almond and pistachio orchards, particularly in organic production. How long specific pathogens survive in manure applied to or incorporated into orchard soil has not been definitively established. When using manure in orchard production, three main aspects should be considered: the source(s) and treatment of the manure, how it is stored on the farm, and how and when it is applied. If raw manure is stored on a farm prior to treatment, or treated on-site, specific procedures to prevent contamination via water, wind, equipment and personnel are needed. The raw manure should be stored as far away as possible from the orchard, preferably with barriers that prevent water runoff from the manure to the orchard, roads to the orchard, or equipment storage areas. The manure should be stored under tarps to prevent wind drift. Once the treated manure can be applied to the orchard, the information on vendor, certified treatments, rate(s) and date(s) of application and incorporation, and location should be recorded.

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15.6.4 Water Managing and monitoring water supplies are among the key processes for preventing microbiological and chemical contamination of almonds and pistachios. Documentation of an orchard’s primary and secondary irrigation supplies should include current source and quality. Typical water sources are ground water from capped and uncapped wells, and surface water from reservoirs, canals, collection ponds, or government water delivery systems. Water is used to irrigate orchards, spray the trees and orchard floor, decrease dust from orchard roads, and clean orchard equipment. Water is also used for hand washing and is consumed by employees. Therefore, water in orchard production can be both a source and a carrier of biological and chemical contamination. To prevent contamination by water in an orchard requires knowing the sources and quality of the water supply, verifying the same with direct testing, and knowing the potential sources of contamination, particularly those over which there is no direct control. Irrigation is the major use, by volume, of water in orchards. Almond and pistachio trees can be irrigated by a variety of methods including flood, furrow, subsurface drip, and microsprinkler. Methods that conserve water (e.g., drip and microsprinkler) are increasingly used in new plantings and virtually all pistachios are irrigated this way (CPRB, 2009). Water used in crop sprays and dust control pose nut crop contamination risks by direct contact with the exposed nut on the tree or by contact with the ground. If there is a potential for contamination of the mature crop on the tree or for almonds on the ground, the best practice is to use only previously tested, ground or municipal water rather than surface water, for spraying, refilling and cleaning spray tanks and equipment. During spraying, field applicators should be trained in hose placement and handling to prevent cross contamination. Many spray application and post-spray equipment sanitation practices are detailed in state and federal pesticide laws. Growers should evaluate whether the water used for orchard dust control during harvest operations has the potential to contaminate the crop. Road spraying should be controlled to prevent splashing into the orchard, particularly onto the nuts or onto ground where nuts will fall. Adjacent land uses including sewage treatment facilities, septic tanks, leach fields, composting, farming or animal operations, and wildlife habitats have the potential for effluent discharge into an orchard’s water conveyance and intake systems. Contamination by these sources is frequently related to weather events, particularly storms. These potential hazards should be noted and, if possible, physical barriers or diversions, such as holding ponds, should be constructed. Almond producers, huller-shellers, and processors should consider the potential increased risks of Salmonella contamination associated with significant wetting of almonds in the field. Almond-specific GAPs should address wetting of prematurely fallen almonds with irrigation water and provide specific guidelines for harvesting rained-on almonds. Huller-shellers and processors may want to consider segregating rained-upon almonds and increasing sanitation procedures after handling these almonds to avoid potential for cross contamination (Uesugi et al., 2006).

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15.6.5 Pest control Control of specific crop pests, primarily insects and nematodes, is typically achieved by chemical applications and, therefore, potentially causes chemical contamination. Chemical use is the most highly regulated practice in almond and pistachio production. Chemicals, other than foliar or inert compounds and fertilizers, must be registered for use on almonds or pistachios for a specific purpose. The storage, transport, use, mixing, application and post application safety practices, including equipment and worker clean-up, are designed to protect workers, non-target insects and animals, and the environment. There are specific regulations for each chemical, but most follow the same format requiring permits to use the chemical, posting of use, application limits, application records for a specified period of time, application by currently certified applicators with documentation of recent training, specific parameters of mixing and loading, and quality monitoring of the water used in applications. Education of other orchard workers on chemical use including safety precautions and emergency procedures is similarly detailed by local, regional and federal regulations. 15.6.6 Orchard floor management Generally, orchard soils would not be tested for microbial pathogens before establishment of an orchard unless previous land use includes a dairy or poultry operation. Even then, evaluating soils prior to planting is not as relevant as it might be for annual crops. There are typically 3 to 4 years from time of planting an almond tree to first harvest; a typical orchard will be maintained for about 25 years (Duncan et al., 2011). For pistachios, times between planting and commercial yields are 5 to 6 years (Beede et al., 2008); maximum yields are expected after 12 to 13 years and well maintained orchards may stay in production for 40 years or more. Orchard soils would rarely be evaluated for the presence of microbial pathogens during production unless a major incident, such as flooding, runoff or leakage from an unusual source, indicates the potential contamination of the harvested crop. Effective orchard floor management will help to reduce microbiological, chemical, and physical contamination of almonds and pistachios. Orchard floor management focuses on characterizing, excluding, preventing or eliminating potential for contamination. Attention should also be paid to developing the best method of decreasing dust within an orchard, preventing trash from accumulating at orchard operations facilities, and regularly inspecting the latter for pest infestation. A defined policy for collecting the garbage and debris produced by workers after eating and drinking in the orchard will help to further reduce the potential for contamination. Sources of animal habitat should be minimized within the orchard and in complementary support facilities by eliminating unwanted vegetation, particularly near water sources. Almonds spend an extended time on the ground after harvest to dry, are moved about on the orchard floor by harvesting equipment, and are mixed repeatedly thus increasing their points of contact with the orchard floor and other nuts. The harvested almonds are also in the direct path of the dusts generated by the shaker

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harvesters and windrowing and collecting machines. For best pick-up of the crop, almond orchard floors should be kept as smooth, clear and dry as possible. Orchard floor preparation is also a factor in how much dust is generated by harvest winnowing and nut collection. Pistachios are harvested by mechanically shaking the tree trunks to drop the nuts into catch frames that enclose the trunk and then convey the nuts into bins or haulers. As a result, orchard floor management is not the same issue for pistachios as the nuts are fully enclosed in fleshy hulls and do not contact the orchard floor. Retrieval of nuts that were not initially caught in the harvester catch frame or that spilled out of the catch frame is not typically permitted.

15.7

Post-harvest options to reduce microbial loads

The ability of Salmonella to survive in the almond production and processing environments and its presence in raw almonds raised concerns about the potential for additional outbreaks (Danyluk et al., 2006) and led to the promulgation of new food safety regulations for this industry in the US, effective 1 September 2007 (USDA, 2007). The regulation requires almonds sold in North America (Canada, US and Mexico) to be treated by a process or processes that achieve, in total, a minimum 4-log reduction in Salmonella. Almonds destined for the North American market are either processed in California or sold to approved users who process the almonds prior to sale. The target level of reduction (4 log) was based, in part, by a risk assessment published the year before the regulation became final that demonstrated little difference between a 5- or 4-log reduction of Salmonella on raw almonds with respect to predicted numbers of illnesses from almonds in the US each year (Danyluk et al., 2006). Lambertini et al. (2012) re-evaluated the risk assessment adding new and additional data and modifying some of the initial assumptions used in 2006. Their conclusions were that salmonellosis from consumption of almonds would be prevented with current industry practices even if prevalence and levels of Salmonella were significantly above those observed in previous surveys. They also evaluated data from the 2001 outbreak and concluded that a relatively small amount of raw almonds with an unusually high prevalence (65%) and low levels (1 MPN/g) of Salmonella was sufficient to cause a major outbreak. The model predicted that if the outbreak almonds had been treated by a process capable of achieving a 4-log reduction in Salmonella the outbreak would likely have been prevented or dramatically reduced. A sensitivity analysis was performed to identify factors that exert the greatest influence on the model. For raw almonds the top three factors were: (1) total handler storage time; (2) reduction occurring during consumer storage (or consumer storage temperature); and (3) consumer storage time (Danyluk et al., 2006). For processed almonds the top two factors were: (1) treatment method; and (2) storage time. Closely-related Salmonella Enteritidis PT 30 or 9c (atypical phage types of Salmonella) were identified as strains associated with three raw almond outbreaks

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(CDC, 2004; Isaacs et al., 2005; Ledet Müller et al., 2007; Parker et al., 2010). Salmonella Enteritidis PT 30 was selected as a target organism for almonds; several post-harvest methods have been evaluated using this organism (Danyluk et al., 2005; Du et al., 2010a; Harris et al., 2012). The increased heat resistance of microorganisms that are in dry foods is well documented albeit not well understood (Archer et al., 1998; Goepfert et al., 1968; McDonough et al., 1968). Moisture and water activity of almonds and relative humidity of the environment have been shown to impact the heat resistance of Salmonella on almonds (Jeong et al., 2011; Kaur and Harris, 2010), with observations of increased sensitivity to heat treatment on almonds at higher moisture levels or at higher relative humidity. Almond treatments that reduce population levels of Salmonella can be separated into two major classifications: (1) those that significantly alter the characteristics of the raw almond (e.g., blanching, various types of roasting); and (2) those that do not significantly alter the characteristics of a raw almond (e.g., propylene oxide, high pressure, infrared heating, moist air impingement, steam or combination treatments) (ABC, 2007a; Bari et al., 2009, 2010; Brandl et al., 2008; Chang et al., 2010; Jeong et al., 2009; Lee et al., 2006; Willford et al., 2008; Yang et al., 2010). A recent review provides an overview of the treatments that have been investigated for use with almonds (Pan et al., 2012) and additional information can be found in Chapters 3 and 7. Commercial blanching is a hot water or steam process carried out to remove the outer pellicle or seed coat (brown skin) of almonds. Blanching consists of multiple steps, including pre-wetting, scalding, peeling, (a series of rubber rollers that facilitate removal of the loosened skins), rinsing (free skins are rinsed away with a water spray) and the wet almonds are dried with forced hot air. Heat is applied at both the scalding and drying steps. A D value of 0.4 min was determined at 88°C for Salmonella Enteritidis PT 30-inoculated almonds in hot water with a z value of 35C° (Harris et al., 2012). A blanching process of 1.6 to 2.0 min at a minimum temperature of 88°C at the cold spot is a recognized process that will ensure a 4- or 5-log reduction, respectively, of Salmonella (ABC, 2007b). Significantly higher temperatures are required to achieve comparable reductions under dry heat conditions. Almonds may be roasted by immersion in hot oil or in various types of dry roasters. In hot oil, the thermal survival curve for Salmonella Enteritidis PT 30-inoculated almonds is an upward concave curve with an asymptotic tail (Du et al., 2010a). The Weibull model, often used to analyze non-linear survival curves, was used to analyze the data and 4-log reductions were calculated to be achieved in 1.4 and 0.74 min at 121 and 127°C, respectively (Du et al., 2010a). Due to the shape of the curve the time to achieve a 5-log reduction was almost double: 2.4 and 1.3 min at 121 and 127°C, respectively. Almonds often are stored for long periods before treatment. Abd et al. (2012) showed that heat resistance of Salmonella did not change over 12 weeks when inoculated almonds were stored at 4°C. For commercially oil-roasted almonds, a minimum of 1.6 or 2.0 min at 127°C is considered necessary to meet the 4-log requirement or a 5-log reduction, respectively (ABC, 2007c).

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Dry roasters and many other types of equipment are difficult to validate using laboratory equipment. On inoculated almonds, Enterococcus faecium strain NRRL B-2354 (E. faecium ATCC8459) has a thermal tolerance in dry and moist heat that is similar to or more conservative than Salmonella Enteriditis phage type 30 (Jeong et al., 2011; Kaur and Harris, unpublished; Theofel and Harris, unpublished). E. faecium NRRL B-2354 is classified as a non-pathogen by the American Type Culture Collection and, therefore, may be considered an appropriate surrogate for on-site validation of thermal processes designed to treat almonds (ABC, 2007d). Propylene oxide (PPO) fumigation has been shown to achieve at least a 5-log CFU/g reduction of Salmonella Enteritidis PT 30 on almond kernels (ABC, 2007a; Danyluk et al., 2005). The lethality of gas treatments of nuts is dependent on concentration, exposure time, exposure temperature, product temperature, humidity, and holding times after the treatment period. The use of PPO is permitted on tree nuts (Crop group 14) in the US (EPA, 2007). The residual content of propylene oxide in processed nut meats is limited to 300 ppm and the residual content of the reaction product, propylene chlorohydrin, is limited to 10.0 ppm at the time the product is shipped. Some countries have not established a tolerance for PPO residues; use of PPO on US nuts for export is restricted to those countries that have established tolerances. Pistachios are treated by many of the same processes used for almonds. Dry roasting is much more commonly used for pistachios than oil roasting; PPO fumigation is also an option. However, published data for pistachios are currently unavailable. Processes validated for almonds cannot be directly used for pistachios; preliminary studies in hot oil and with PPO indicate that for pistachios increased processing times or concentrations are needed for equivalent target reductions in Salmonella (Theofel and Harris, unpublished). Application of a validated process to reduce Salmonella or other pathogens in almonds or pistachios is only effective if the post-processing contamination is prevented. Sanitation in dry facilities is a challenge (Chen et al., 2009a; Du et al., 2007, 2010b) but critical to protecting the product. Salmonella survive well and for long periods of time in processing facilities (Isaacs et al., 2005; Russo et al., 2013). Recalls of Salmonella-contaminated roasted tree nuts have been documented (FDA, 2009; Little et al., 2009). In addition to appropriate sanitation programs and segregation policies, environmental monitoring programs are considered an essential part of Salmonella control (Chen et al., 2009b; GMA, 2009).

15.8

Composition

Almonds and pistachios are rich in important macronutrients including plant protein, dietary fiber and monounsaturated fatty acids, and low in saturated fat. Table 15.4 provides a summary of selected composition data for California almonds and pistachio nuts including the commonly consumed dry roasted forms, as adapted from the US Department of Agriculture National Nutrient Database

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Nutrient composition (per 100 g) of almonds and pistachios

Nutrients

Proximates Energy Water Protein Lipids (total) Saturated fatty acids (total) Monounsaturated (total) Polyunsaturated (total) Dietary fiber (total) Sugars (total) Minerals Calcium Iron Magnesium Phosphorus Potassium Sodium Zinc Copper Manganese Vitamins Thiamin Riboflavin Niacin Folate, food Carotene, beta Lutein + zeaxanthin Vitamin B6 Vitamin E (alphatocopherol) Tocopherol, gamma

Units

Almonds, Almonds, Pistachio Pistachio nuts, natural dry roasted nuts (raw) dry roasted (with skin) (unsalted) (unsalted)

kcal g g g g

575 4.70 21.22 49.42 3.73

595 2.53 21.06 52.05 4.03

562 3.91 20.27 45.39 5.56

5 67 1.85 20.95 44.82 5.46

30.89 12.07 12.20 3.89

32.38 13.00 10.90 4.93

23.82 13.74 10.3 7.66

23.68 13.45 9.9 7.74

mg mg mg mg mg mg mg mg mg

264 3.72 268 484 705 1 3.08 1.00 2.29

267 3.83 281 470 712 3 3.30 1.11 2.31

105 3.92 121 490 1025 1 2.20 1.30 1.20

107 4.03 109 469 1007 6 2.34 1.29 1.24

mg mg mg μg μg μg mg mg

0.21 1.01 3.39 50 1 1 0.14 26.22

0.08 0.97 3.55 53 1 1 0.13 23.80

0.87 0.16 1.30 51 249 1405 1.70 2.30

0.70 0.23 1.37 51 156 1160 1.12 2.42

mg

0.65

0.68

22.60

23.56

g g g g

Source: Adapted from USDA National Nutrient Database for Standard Reference, Release 25 (2012).

(USDA, 2012). The USDA nutrient data sets for almonds represent a comprehensive multi-year sampling of the major California almond varieties. Both tree nuts are a good food source of many essential minerals such as magnesium, iron, phosphorus, potassium, zinc, copper and manganese. Almonds are an excellent source of alpha-tocopherol, which is the most biologically active form of vitamin E. Tocopherols are important antioxidants and pistachios are rich in gamma-tocopherol. Pistachios are unique among tree nuts in being a source of carotenoids including beta-carotene, lutein and zeaxanthin. After harvest, almonds and pistachios have a stable composition and a long shelf life under cool and dry storage and handling conditions due to the nuts’ low

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moisture level (below 6%) and high content of natural antioxidants. Roasted nuts are susceptible to oxidation and must be protected from oxygen. Almond shells provide limited soluble sugar (0.35%), fat (0.41%), protein (1.0%) and ash (0.69%) on a dry weight basis (Saura-Calixto et al., 1983) compared to hulls, which have higher levels of soluble sugar (26.55%), fat (3.34%), protein (2.7%) and ash (6.09%) (Saura-Calixto and Cañellas, 1982). The dominant soluble sugars found in almond hulls are sucrose (40%), glucose (23%) and fructose (17%).

15.9

Future trends

The 2000–2001 outbreak of salmonellosis associated with raw almonds was the first well investigated outbreak of foodborne illness linked to tree nuts (Isaacs et al., 2005). Since that time, significant data have become available on almonds and many other tree nuts that have aided these industries in establishing sciencebased food safety programs. The market for all tree nuts continues to expand worldwide which has led to significant increases in almond and pistachio production. Production by the California almond and pistachio industries alone has more than doubled between 2000 and 2013. This expansion has led to increased system-wide pressures during harvest. Although Salmonella is well established as the pathogen of concern in lowmoisture foods, recent outbreaks of E. coli O157:H7 gastroenteritis epidemiologically linked to hazelnuts (CDC, 2011) and walnuts (PHAC, 2011) suggest that this organism should also be considered in almond and pistachio food safety plans. Data on survival of this organism on almonds and pistachios during storage (Kimber et al., 2012) and preliminary data with oil roasting (Theofel and Harris, unpublished) suggest that Salmonella-control programs should also be effective in controlling E. coli O157:H7. In January of 2013 the US FDA published two proposed rules that apply to almonds and pistachios. The Produce Safety Rule (FDA, 2013a) covers pre-harvest and harvest activities and the Preventative Controls Rule (FDA, 2013b) covers post-harvest activities. The final rules, anticipated in 2014, will likely require updating and enhancement of almond and pistachio food safety plans.

15.10 Sources of further information and advice For additional information see a publication by the Grocery Manufacturers Association on developing food safety programs for nuts (GMA, 2010), Lee et al. (2011) for information on consumer handling of tree nuts, Pan et al. (2012) for a review of processes to reduce microorganisms on almonds, and a series of publications by Scott et al. (2009) and Chen et al. (2009a, 2009b) that outline control of Salmonella in low-moisture foods.

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15.11 References (2007a), Pasteurization treatments. Available from: http://www.almondboard.com/ Handlers/Documents/Pasteurization-Treatments.pdf [Accessed 1 December 2012]. ABC (2007b), Guidelines for validation of blanching processes. Available from: http:// www.almondboard.com/Handlers/FoodQualitySafety/Pasteurization/Pasteurization Program/ValidationGuidelines/ [Accessed 1 December 2012]. ABC (2007c), Guidelines for validation of oil roasting processes. Available from: http:// www.almondboard.com/Handlers/FoodQualitySafety/Pasteurization/Pasteurization Program/ValidationGuidelines/ [Accessed 1 December 2012]. ABC (2007d), Guidelines for process validation using Enterrococcus faecium NRRL B-2354. Available from: http://www.almondboard.com/Handlers/FoodQualitySafety/Pasteurization/ PasteurizationProgram/ValidationGuidelines/ [Accessed 1 December 2012]. ABC (2009), Good agricultural practices for almond growers, Almond Board of California. Available from: http://www.gmaonline.org/downloads/wygwam/Addendum_3_GAP_ for_Almond_Growers.pdf [Accessed 1 February 2013]. ABC (2012), 2012 Almond almanac, Almond Board of California. Available from: http:// www.almondboard.com [Accessed 1 February 2013]. ABD S J, MCCARTHY K L and HARRIS L J (2012), ‘Impact of storage time and temperature on thermal inactivation of Salmonella Enteritidis PT 30 on oil-roasted almonds’, J Food Sci, 77, M42–M47. AGUILAR A A, SMITH N E and BALDWIN R L (1984), ‘Nutritional value of almonds hulls for dairy cows’, J Dairy Sci, 67, 97–103. ARCHER J, JERVIS E T, BIRD J and GAZE J E (1998), ‘Heat resistance of Salmonella weltevreden in low-moisture environments’, J Food Prot, 61, 969–973. BANSAL A, JONES T M, ABD S J, DANYLUK M D and HARRIS L J (2010), ‘Most-probable-number determination of Salmonella levels in naturally contaminated raw almonds using two sample preparation methods’, J Food Prot, 73, 1986–1992. BARI M L, NEI D, SOTOME I, NISHINA I, ISOBE S and KAWAMOTO S (2009), ‘Effectiveness of sanitizers, dry heat, hot water, and gas catalytic infrared heat treatments to inactivate Salmonella on almonds’, Foodborne Pathog Dis, 6, 953–958. BARI M L, NEI D, SOTOME I, NISHINA I, HAYAKAWA F et al. (2010), ‘Effectiveness of superheated steam and gas catalytic infrared heat treatments to inactivate Salmonella on raw almonds’, Foodborne Pathog Dis, 7, 845–850. BEEDE R H, KALLSEN C E, HOLTZ B A, FERGUSON L, KLONSKY K M and DE MOURA R L (2008), Sample costs to establish and produce pistachios: San Joaquin Valley South, University of California Cooperative Extension. Available from: http://coststudies.ucdavis.edu/ files/PistachioVS08.pdf [Accessed 1 February 2013]. BEUCHAT L R and MANN D A (2010), ‘Factors affecting infiltration and survival of Salmonella on in-shell pecans and pecan nutmeats’, J Food Prot, 73, 1257–1268. BLESSINGTON T, MITCHAM E J and HARRIS L J (2012), ‘Survival of Salmonella enterica, Escherichia coli O157:H7, and Listeria monocytogenes on inoculated walnut kernels during storage’, J Food Prot, 75, 245–254. BRANDL M T, PAN Z, HUYNH S, ZHU Y and MCHUGH T H (2008), ‘Reduction of Salmonella Enteritidis population sizes on almond kernels with infrared heat’, J Food Prot, 71, 897–902. CAMPBELL B C, MOLYNEUX R J and SCHATZKI T F (2003), ‘Current research on reducing preand post-harvest aflatoxin contamination of US almond, pistachio, and walnut’, Toxin Rev, 22, 225–266. CANDLISH A A G, PEARSON S M, AIDOO K E, SMITH J E, KELLY B and IRVINE H (2001), ‘A survey of ethnic foods for microbial quality and aflatoxin content’, Food Addit Contam, 18, 129–136. (CDC) CENTERS FOR DISEASE CONTROL AND PREVENTION (2004), ‘Outbreak of Salmonella serotype Enteritidis infections associated with raw almonds – United States and Canada, 2003–2004’, MMWR Weekly, 53, 484–487. ABC

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