Nuts have been identified as a vector for salmonellosis. The objective of this project was to estimate the prevalence and contamination level of Salmonella in raw tree nuts (cashews, pecans, hazelnuts, macadamia nuts, pine nuts, and walnuts) at retail markets in the United States. A total of 3,656 samples of six types of tree nuts were collected from different types of retail stores and markets nationwide between October 2014 and October 2015. These samples were analyzed using a modified version of the Salmonella culture method from the U.S. Food and Drug Administration's Bacteriological Analytical Manual. Of the 3,656 samples collected and tested, 32 were culturally confirmed as containing Salmonella. These isolates represented 25 serotypes. Salmonella was not detected in pecans and in-shell hazelnuts. Salmonella prevalence estimates (and 95% confidence intervals) in cashews, shelled hazelnuts, pine nuts, walnuts, and macadamia nuts were 0.55% [0.15, 1.40], 0.35% [0.04, 1.20], 0.48% [0.10, 1.40], 1.20% [0.53, 2.40], and 4.20% [2.40, 6.90], respectively. The rates of Salmonella isolation from major or big chain supermarkets, small chain supermarkets, discount, variety, or drug stores, and online were 0.64% [0.38, 1.00], 1.60% [0.80, 2.90], 0.00% [0.00, 2.40], and 13.64% [2.90, 35.00], respectively (Cochran-Mantel-Haenszel test: P = 0.02). The rates of Salmonella isolation for conventional and organic nuts were not significantly different. Of the samples containing Salmonella, 60.7% had levels less than 0.003 most probable number (MPN)/g. The highest contamination level observed was 0.092 MPN/g. The prevalence and levels of Salmonella in these tree nut samples were comparable to those previously reported for similar foods.

Nuts (tree nuts and peanuts) have low water activity and thus do not provide favorable conditions for bacterial growth. However, Salmonella has been detected in pecans, peanuts, almonds, pistachios, walnuts, and pine nuts during the last few years (57, 9, 10, 15, 16, 22, 24), Escherichia coli O157:H7 has been found in peanuts, pecans, and walnuts (8, 16, 24), and Listeria monocytogenes has been found in peanuts, pecans, and mixed nuts (8, 17). Bacteria such as Pseudomonas, Clostridium spp., and Klebsiella spp. with potential health risks especially for young and immunocompromised people have also occasionally been found in nuts (3, 4). Many species of Aspergillus, including about 40 that have been implicated in human or animal infections, can infect and cause decay in nuts. Some Aspergillus species produce aflatoxin, which is both a toxin and a carcinogen (4). The presence of such contaminants in nuts could cause human health problems.

At least 25 recalls were issued in 2015 in the United States due to Salmonella contamination of walnuts, pecans, macadamia nuts, pine nuts, almonds, and hazelnuts (26). Worldwide, numerous outbreaks of foodborne illness in recent years have been associated with almonds, cashews, hazelnuts, pine nuts, pistachios, and walnuts; a majority of these outbreaks were caused by Salmonella infection. For example, raw almonds contaminated with Salmonella Enteritidis caused 29 illnesses in Canada and 12 states in the United States during 2003 and 2004 (11). Recently, an outbreak of Salmonella Montevideo infection involving nine states was associated with pistachios (13). These events have raised concerns about the public health risk associated with consumption of tree nuts. Basic information, such as the extent of contamination and type of nuts contaminated, could provide important information to inform the development of mitigation strategies to reduce public health risks associated with consumption of nuts.

The objective of this study was to estimate the prevalence and level of Salmonella in tree nuts at retail markets in the United States. This information will assist the U.S. Food and Drug Administration (FDA) in the development of a quantitative assessment of the risk of human salmonellosis associated with the consumption of tree nuts in the United States (29). The tree nuts included in the study were selected to provide information on Salmonella prevalence and level for nuts where limited information was available, such as for cashews, pecans, hazelnuts, macadamia nuts, pine nuts, and walnuts. This study will help to fill some of the data gaps in the risk assessment of salmonellosis from consumption of tree nuts in the United States.

Sample collection.

A commercial testing laboratory under contract with the FDA between 6 October 2014 and 21 October 2015 collected and analyzed 3,656 samples of tree nuts: raw cashews (shelled), pecans (shelled), hazelnuts (shelled and in shell), macadamia nuts (shelled), pine nuts (shelled), and walnuts (shelled) (Table 1). To be as representative as possible, the collection sites were selected using U.S. Census Bureau maps (28) for California (West Region, Pacific Division), Colorado (West Region, Mountain Division), Connecticut (Northeast Region, New England Division), Georgia (South Region, South Atlantic Division), Maryland (South Region, South Atlantic Division), Minnesota (Midwest Region, West North Central Division), Texas (South Region, West South Central Division), Washington (West Region, Pacific Division), Illinois (Midwest Region, East North Central Division), North Carolina (South Region, South Atlantic Division), and Vermont (Northeast Region, New England Division).

TABLE 1.

Tree nut sample characterization and Salmonella prevalence

Tree nut sample characterization and Salmonella prevalence
Tree nut sample characterization and Salmonella prevalence

Samples were selected from different types of retail markets categorized as (i) major chain or big chain supermarkets, both national and regional; (ii) small chain or independent organic and specialty supermarkets, including retail outlets; (iii) discount, variety, or drug stores and discount stores, including large discount clubs such as Costco, BJ's, and Sam's Club and smaller discount stores such as Dollar stores and other retail outlets for which foods are just a fraction of their business, including national and regional drug stores and gas stations; and (iv) online Internet retail sellers (for a very limited number of samples of macadamia nuts that were difficult to obtain in regular retail stores). Numbers of samples collected from each category of market and numbers of unique addresses visited when collecting samples are listed in Table 2. In most cases, the minimum sample size was 800 g. For a few samples for which it was difficult to obtain the required amount from a single lot (i.e., available packages with same lot or date), 500 g of nuts were purchased as one sample. Only prepacked (e.g., jars, bags, or cans) tree nuts were collected. Samples were not repackaged when purchasing to avoid cross-contamination. Bagged samples remained sealed before microbiological analysis was conducted. Nuts in open bins for self-serve by consumers and nuts in displays were excluded. Whenever multiple retail sale units were required to attain a sufficient sample size, all units were from the same lot and were placed in one plastic zip-style bag. Valid samples consisted of raw whole nuts, halves, or pieces or nuts that were diced or chopped. Nuts that had been roasted or were coated with seasonings, chocolate, or other candy were excluded. Nut butters, nut pastes, nut meals, nut flours, and mixed nuts were also excluded. Valid samples required a unique identifier for the producer, grower, or distributor and a “use-by” or “sell-by” date and/or lot number. Collected samples were held at 4°C until used for microbiological analysis.

TABLE 2.

Retailer collection sites and Salmonella prevalence by retailer type

Retailer collection sites and Salmonella prevalence by retailer type
Retailer collection sites and Salmonella prevalence by retailer type

Microbiological assay.

The sample size used for testing for the presence of Salmonella in nuts was 375 g. The nut to preenrichment broth ratio was kept at 1:9 (w/v). Salmonella detection, isolation, and confirmation from nuts were accomplished using a modification of the method described in the FDA's Bacteriological Analytical Manual (BAM) (30) by replacing lactose broth with buffered peptone water.

Salmonella levels in nut samples that tested positive were estimated with a three-tube five-dilution (100, 10, 1.0, 0.1, and 0.01 g) most-probable-number (MPN) method (31) and the BAM Salmonella method. For a few samples for which it was difficult to obtain the required amount of nuts from a single lot, the three-tube 100-g dilution series was not analyzed. This exception applied to a few pine nut samples where the quantities available for retail purchase were so small that 800 g could not be obtained from a single lot.

Serotyping Salmonella.

Salmonella isolates were serotyped using the Luminex xMAP Salmonella serotyping assay (23). Isolates that were untypeable with this assay were serotyped using the conventional Kauffman-White antigenic formulae scheme (19, 30).

PFGE.

Pulsed-field gel electrophoresis (PFGE) laboratory analysis followed the official PulseNet protocol (14). XbaI was utilized as the primary restriction enzyme, and BlnI was used as the secondary restriction enzyme.

Genome sequencing.

Isolates obtained were grown in tryptic soy broth (Difco, BD, Franklin Lakes, NJ) overnight at 37°C, and genomic DNA was extracted using the DNeasy blood & tissue kit (Qiagen, Valencia, CA). DNA concentrations were measured with a Qubit fluorometer (Life Technologies, Carlsbad, CA), standardized to 0.2 ng/μL, and stored at −20°C until library preparation. Libraries were prepared with the Nextera XT DNA sample preparation kit (Illumina, San Diego, CA) according to the manufacturer's instructions. Genomes were sequenced using the MiSeq sequencing technology (Illumina) with 500 (2 × 250) cycles and the pair-end library with coverage depth of 30 to 90× at the FDA Center for Food Safety and Applied Nutrition genomics laboratory. All genomes were submitted as assembled reads to the National Center for Biotechnology Information (NCBI) (2).

Statistical analysis.

Confidence intervals for prevalence were derived using the Clopper and Pearson procedure, prevalences were compared using Fisher's exact test, and the Cochran-Mantel-Haenszel (CMH) chi-square test was used to test the conditional independence of a factor (conventional versus organically grown, types of retail) for each tree nut type (1). Statistical analyses were performed using R software (27).

Salmonella prevalence.

Of the 3,656 nut samples collected and tested, 32 were confirmed by culture as containing Salmonella. Information about these samples is provided in Table 1. Salmonella was not detected in pecans (623 samples) or in-shell hazelnuts (80 samples). Salmonella prevalence in cashews, shelled hazelnuts, and pine nuts was 0.55% (4 of 733 samples), 0.35% (2 of 577 samples), and 0.48% (3 of630 samples), respectively. Salmonella prevalence in walnuts was 1.22% (8 of 658 samples). Macadamia nuts had the highest Salmonella prevalence among all six types of nuts tested, at 4.23% (15 of 355 samples). Of the 18 macadamia samples purchased online, 3 were positive for Salmonella. Even without the 18 online samples, the prevalence in macadamia nuts was 3.60%, still the highest among the six nut types studied. These data were similar to limited published reports on Salmonella contamination in various varieties of tree nuts in the United States, including almonds, pecans, walnuts, and pistachios. Brar et al. (9) tested Salmonella in in-shell pecans over four harvest years. Salmonella prevalence ranged across years from 0.47 to 1.40%, with an average of 0.95%. Danyluk et al. (15) reported a Salmonella prevalence in raw California almonds of 0.87%. In-shell California walnuts had an average annual Salmonella prevalence of 0.14% (16). Harris et al. (20) reported 0.61% Salmonella prevalence in 3,966 in-shell pistachio samples collected during 2010, 2011, and 2012 in California. Internationally, a 3-year survey of 921 samples of preroasted peanuts, almonds, cashews, hazelnuts, and Brazil nut kernels received at three Australian nut-processing facilities revealed one Salmonella-positive raw almond sample. Salmonella prevalence among almonds and all nuts was 1.67 and 0.11%, respectively (18). In England, one pistachio sample was positive for Salmonella among a total of 727 edible roasted nut kernels (almonds, Brazil nuts, cashews, hazelnuts, macadamia nuts, peanuts, pecans, pine nuts, pistachios, walnuts, tiger nuts, and mixed nuts) on retail sale, for a Salmonella prevalence of 4 and 0.14% for pistachios and for all nuts, respectively (22). These findings of Salmonella-positive nut samples after roasting treatments indicates the importance of validating Salmonella-reduction treatments and implementing controls to minimize recontamination after such treatments to adequately reduce the risk from Salmonella in nuts.

Efforts were made to collect organically grown samples. Except for cashews (181 samples tested), fewer than 50 organic samples were obtained for each of hazelnuts, macadamia nuts, pecans, pine nuts, and walnuts because of their limited availability in the markets. However, 326 organic nut samples from the six types of nuts combined were collected and analyzed for Salmonella, accounting for 8.92% of the total number of samples collected. Two isolates were recovered from organic nuts; thus, the prevalence of Salmonella in organic nuts was 0.61% (Table 1). Overall, the difference in Salmonella prevalence between conventional and organically grown tree nuts was not significantly different (CMH test, P = 0.74). We are unaware of any published data on Salmonella prevalence and levels in organically grown nuts.

Numbers of samples collected from major or big chain supermarkets, small chain supermarkets, discount, variety, or drug stores, and online retailers were 2,800, 685, 149, and 22, respectively (Table 2). A total of 624 unique location addresses were visited during the sample collection process in an effort to sample as many sites as possible to make the result more representative of nuts across the United States. Among the 32 Salmonella strains isolated from the 3,656 nut samples, 18, 11, 0, and 3 were from major or big chain supermarkets, small chain supermarkets, discount, variety, or drug stores, and online retailers, respectively. Corresponding prevalences were 0.64, 1.60, 0, and 13.64, respectively (Table 2). Overall, the proportion of positive samples per type of retail outlet was significantly different (CMH, P = 0.01). The Salmonella prevalence in online samples was higher than that for samples from other retailers (Fisher's exact test, P < 0.01). Two of the three positive samples from online purchases of macadamia nuts were bought on the same day and originated from the same producer (but the lot numbers were different).

Tree nut samples were collected all year, and Salmonella-positive nuts were detected throughout the year (Table 3). However, because typically only one tree nut production cycle occurs per year and information was not available as to the production year or length of storage for each tree nut sample, the finding of Salmonella-positive samples throughout the sampling period provided no additional insights into Salmonella contamination of tree nuts. Collection of data over multiple years would provide a better understanding of Salmonella prevalence and levels in these tree nuts by elucidating yearly variability.

TABLE 3.

Serotypes and PFGE patterns of Salmonella isolates from tree nuts and their NCBI accession numbers

Serotypes and PFGE patterns of Salmonella isolates from tree nuts and their NCBI accession numbers
Serotypes and PFGE patterns of Salmonella isolates from tree nuts and their NCBI accession numbers

Salmonella levels.

Salmonella levels were determined for 28 of the 32 confirmed positive samples. Because of the very low Salmonella levels, enumeration was conducted using the MPN method, which requires a relatively large sample size. For 4 of the 32 samples, too few nuts were available for MPN enumeration. The values for the remaining 28 samples ranged from <0.003 to 0.092 MPN/g: 60.7% had below the limit of detection of 0.003 MPN/g; 25% had 0.003 to 0.005 MPN/g; and the remaining 14.3% had 0.005 to <0.095 MPN/g (Fig. 1). The highest level observed was 0.092 MPN/g in one sample of macadamia nuts ordered online, corresponding to 2.3 MPN/25 g of sample. The two Salmonella-positive organically grown nut samples were macadamia nuts and walnuts, with levels of 0.0092 and <0.003 MPN/g, respectively (data not shown).

FIGURE 1.

MPN results for Salmonella in contaminated nut samples.

FIGURE 1.

MPN results for Salmonella in contaminated nut samples.

Close modal

Kirk et al. (21) tested 142 unopened packets of flavored peanuts and roasted peanuts in Australia, Canada, England, and Wales for the presence of Salmonella and concluded that the Salmonella levels was generally very low, <0.03 to ∼2 cells per gram of peanuts in the shell. Calhoun et al. (10) determined that the Salmonella level in raw shelled peanuts was <0.03 to 2.4 MPN/g. Danyluk et al. (15) reported Salmonella levels in raw California almonds of 1.2 to 2.9 MPN/100 g. The levels of Salmonella in contaminated in-shell California walnuts were estimated at 0.32 to 0.42 MPN/100 g (16). In raw California in-shell pistachios, Harris et al. (20) observed Salmonella levels of 0.10 to 5.3 MPN/100 g.

Serotypes and PFGE profiles of Salmonella isolates from tree nuts.

Serotypes of Salmonella isolates from these tree nuts were very diverse (Table 3); 25 serotypes were identified among the 32 isolates. The majority of the serotypes were isolated only once from the 3,656 samples tested. However, five serotypes were isolated more than once. Salmonella Thompson was isolated from four samples, three of which were walnuts. Salmonella Muenchen was isolated from two walnut samples. Salmonella Plymouth, Salmonella II 42:r:− (also called II Nairobi), and Salmonella Orientalis were each isolated from two different macadamia nuts samples. Among the 25 serotypes, Salmonella Typhimurium, Salmonella Heidelberg, and Salmonella Muenchen were on the Centers for Disease Control and Prevention 2015 top 10 culture-confirmed Salmonella infections list (12).

Calhoun et al. (10) recovered 22 Salmonella isolates belonging to 12 serotypes from raw shelled peanut samples. Kirk et al. (21) found Salmonella Stanley, Salmonella Newport, Salmonella Kottbus, Salmonella Lexington, and an unnamed serotype in 142 unopened packets of flavored peanuts and roasted peanuts from Australia, Canada, England, and Wales. Danyluk et al. (15) obtained 81 Salmonella isolates belonging to 35 serotypes from raw California almonds over a 5-year period. Harris et al. (20) found Salmonella Montevideo in 44% of their contaminated in-shell pistachio samples. Compared with previous surveys, our results, with 25 Salmonella serotypes among 32 isolates (Table 3), were more diverse. The difference could be owing to the fact that previous studies focused on only one type of nut, whereas we evaluated six types. However, even within a single nut type we found a high diversity of serotypes, e.g., 12 serotypes in 15 contaminated macadamia nut samples and 5 serotypes in 8 contaminated walnut samples. We also collected samples at many different locations and in retail stores and markets nationwide, which may have contributed to the Salmonella diversity seen in this study. This diversity of Salmonella is also reflected in the PFGE patterns (Figs. 2 and 3).

FIGURE 2.

PFGE profiles of Salmonella isolates from tree nuts using the restriction enzyme XbaI.

FIGURE 2.

PFGE profiles of Salmonella isolates from tree nuts using the restriction enzyme XbaI.

Close modal
FIGURE 3.

PFGE profiles of Salmonella isolates from tree nuts using the restriction enzyme BlnI.

FIGURE 3.

PFGE profiles of Salmonella isolates from tree nuts using the restriction enzyme BlnI.

Close modal

Genomic sequences of Salmonella isolates from tree nuts.

Sequencing data of most isolates from this project are available from the NCBI database (accession numbers listed in Table 3). The closest relative for each isolate can be found in the subtree based on single nucleotide polymorphisms (25).

Salmonella was not detected on pecans and in-shell hazelnuts. The prevalence of Salmonella on cashews, shelled hazelnuts, pine nuts, and walnuts was similar at 0.35 to 1.22%. Higher prevalences of Salmonella were found on macadamia nuts (4.2% [2.40, 6.90]). In 61% of contaminated samples, the Salmonella levels were below 1 MPN/100 g. The highest level was found in one macadamia nut sample with an estimated 9 MPN/100 g. These results confirm that the presence of Salmonella on tree nuts continues to pose a challenge to the food industry. The 25 different Salmonella serotypes found among the 32 positive samples suggest different contamination sources. To our knowledge, this study is the first in which prevalence and contamination level data have been collected for Salmonella on tree nuts at the retail level in the United States. These data are important for the development of quantitative microbial risk assessments and more specifically will assist the FDA in estimating the risk of human salmonellosis arising from the consumption of tree nuts in the United States.

Mention of trade names or commercial products in the paper is solely for the purpose of providing scientific information and does not imply recommendation or endorsement by the FDA.

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