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LACORS/HPA Co-ordinated Food Liaison Group Studies: Assessment of the Microbiological Safety of Edible Nut Kernels on Retail Sale
in the UK with a focus on Salmonella spp. C.L. Little*1, N Rawal1, E de Pinna1, J McLauchlin2 and the Food, Water and Environmental
Surveillance Network†.
1, Department of Gastrointestinal, Emerging and Zoonotic Infections, Health Protection
Agency Centre for Infections, 61 Colindale Avenue, London NW9 5EQ, UK
2, Health Protection Agency Regional Microbiology Network, London, WC1V 7PP
*, Corresponding author, †, FWES Network comprises Laboratories listed in Annex 1
On behalf of the Local Authorities Co-ordinators of Regulatory Services and the Health Protection Agency
2
Summary
Consumption of nut kernels has shown an upward trend due to people’s increasing tendency
to eat healthy snacks and consumers show a clear preference for shelled nuts (kernels) that
are easy to eat. There is however little published information on the microbiological safety of
this product at retail. A UK study from October 2008 to March 2009 was therefore
undertaken by the HPA and LACORS. A total of 2,886 nut kernel samples of different
varieties were examined for Salmonella spp. and Escherichia coli (an indicator of faecal
contamination) using HPA National Standard Food Methods.
Overall Salmonella spp. and E. coli were detected from 0.1% and 0.8% of edible nut
kernels, respectively. Of the nut kernel varieties examined, S. Senftenberg and S.
Tennessee were detected from two pre-packed samples of Brazil nuts (0.4%) and S.
Anatum from a pre-packed mixed nuts sample (0.9%; mix: almonds, brazils, cashews,
peanuts, walnuts) indicating a risk to health. The levels of Salmonella ranged from <0.01 –
0.23/g. The presence of Salmonella is unacceptable in edible kernels and the Food
Standards Agency was immediately informed and full investigations undertaken.
E. coli at unsatisfactory levels (150/g) was present in another pre-packed Brazils nuts
sample (0.2%). E. coli was additionally found at lower levels (range: 3.6 – 43/g) in Brazils
(1.9%), macadamia (1.5%), pistachios (1.1%), walnuts (0.7%), peanuts (0.7%), hazels
(0.5%), cashews (0.4%), and almonds (0.3%). Levels of E. coli did not correlate with the
presence of Salmonella.
Prevention of microbial contamination in these products lies in the application of good
agricultural, manufacturing and storage practices together with the hazard analysis and
critical control points (HACCP) system that encompass all stages of production, processing
and distribution.
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Introduction The edible nut trade comprises a group of primarily tree crops, grown in both tropical and
temperate regions. Consumption of edible nut kernels has shown an upward trend in the
EU. In 2006, consumption of edible nuts was 2.2 million tonnes, an increase of 10%
compared to 2002. Peanuts and almonds account for half of the consumption, but luxury
nuts such as cashews and macadamias have also increased (CBI, 2008). Consumption of
other nuts such as walnuts, hazlenuts, and Brazils is mainly seasonal, with highest
consumption around Christmas (Wareing et al., 2000). The edible nut sector has clearly
benefited from people’s increasing tendency to eat healthy snacks and consumers also
show a clear preference for ready-shelled nuts (kernels) (CBI, 2008).
At harvest, if good agricultural and hygiene practices are followed, nuts are harvested
with minimal damage and then dried to a water activity of less than 0.7. Finished nut kernel
products may be either treated with chemical preservatives or heat processed and/or packed
in hermetically sealed containers (CAC, 1972; Wareing et al., 2000). The Codex
International Code of Hygienic Practice for tree nuts states that these products should be
free from pathogenic microorganisms (CAC, 1972).
Although nut-associated outbreaks of infection are relatively uncommon, recent
outbreaks of salmonellosis associated with the consumption of peanuts, peanut products,
and almonds have raised awareness of nuts as a potential vehicle for foodborne illness
(CDC 2004, 2009a; Isaacs et al. 2005; Kirk et al. 2004; Ledet Muller et al. 2007).
Salmonella cannot multiply on nuts, but can survive on and in these products for more than
one year (Uesugi et al. 2006) and has been isolated from nut kernels, such as peanuts (Kirk
et al. 2004), almonds (Danyluk et al. 2007; Eglezos et al. 2008), pistachios (CDC 2009b;
Little et al. 2009), cashews and Brazils (Freire and Oxford 2002).
There is little published data on the contamination of edible nut kernels with
Salmonella spp. Surveys of almonds in the USA have been performed following outbreaks of
Salmonella associated with the consumption of these nuts in the early 2000s. For example,
Danyluk et al. (2007) examined 9,274 almond samples from almond processors from 2001
to 2005. Of these, 81 (0.9%) were found to be contaminated with 35 different serotypes of
Salmonella. A survey of a variety of pre-roasted nuts sampled at nut processing facilities in
Australia between 2003 and 2006 found Salmonella in one raw almond sample (1.7%, 1/60)
(Eglezos et al. 2008).
A Health Protection Agency (HPA) study took place in early 2008 to provide a rapid
assessment of the microbiological safety of 727 edible nut kernels on retail sale in England.
Of the nut varieties examined, S. Havana was detected from one sample (4.0%, 1/25) of
pistachio nuts, indicating a risk to health (Little et al., 2009). The HPA study took place
following concerns raised by the detection of Salmonella spp. in 23 (0.6%) of 3,735 edible
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dried seed samples in a 2007/8 Local Authorities Co-ordinators of Regulatory Services
(LACORS)/HPA study (a similar product to edible nut kernels) (Willis et al. 2009), and also
the detection of S. Schwarzengrund in a Brazil nut confectionery product produced in the UK
in 2007 (Anon, 2007). These findings demonstrate that edible kernels are also a potential
source of microbial contamination in the UK.
In response to these investigations, the LACORS/HPA Co-ordinated Food Liaison
Group programme undertook a microbiological study with the aim of assessing the
microbiological safety of edible nut kernels on retail sale in the UK, with a particular focus on
the detection of Salmonella species. A range of edible nut kernels were sampled and
examined over a six month period to provide further data on the microbiology of these
products and to highlight potential problems with their production and use.
Materials and Methods
Sample Collection
A total of 2,886 edible nut kernel samples collected from retail premises were examined by
27 Official Control Laboratories across the UK from 1 October 2008 to 31 March 2009.
This included pistachio nuts that had the shell open (i.e. not wholly shelled). Kernels
collected were retailed as a ready-to-eat snack food. Edible kernels coated with chocolate,
yoghurt or other coatings, flavoured with seasonings (spices, salt, etc.) were specifically
excluded from the study.
Registered retail premises lists held by Local Authority (LA) Environmental Health
Departments (EHDs) were used to derive an approach to sampling. Retail premises were
selected at random from LAs’ database of food businesses via a random number generator.
Samples (≥150g) were collected and transported to laboratories by sampling officers from
265 EHDs, involving 49 Local Authority Food Liaison Groups (Annex 1), in accordance with
the Food Standards Agency (FSA) Food Law Code of Practice (FSA, 2008a) and the Local
Authorities Co-ordinators of Regulatory Services (LACORS) guidance on microbiological
food sampling (LACORS, 2006). Information on samples was recorded on a standard
questionnaire (Annex 2).
Sample Examination
Escherichia coli was enumerated and the presence of Salmonella sought in accordance with
HPA Standard Methods F22 and F13 respectively (HPA, 2005; HPA, 2008). Where
Salmonella was detected, Salmonella was also enumerated by a Most Probable Number
(MPN) 10-tube method. This involved preparing a 1 in 10 dilution of the sample by adding
900 ml of Buffered Peptone Water to 100 g of sample. Ten aliquots, each of 100 g, of this
5
homogenate were then dispensed into separate sterile containers. These were incubated
and sub-cultured as described in HPA Standard Method F13 (HPA, 2008). The number of
aliquots from which Salmonella was detected was compared to a MPN 10-tube table
(adapted from ISO/FDIS 7218:2007 (ISO, 2007)). All isolates of Salmonella were sent to
the Laboratory of Gastrointestinal Pathogens (LGP), HPA Centre for Infections, for further
characterisation. This included sero-typing (Bale et al., 2007; Popoff and Le Minor, 2001)
and antimicrobial sensitivity testing (Frost, 1994).
Microbiological results were compared to Guidelines for the microbiological quality of
some ready-to-eat foods sampled at the point of sale (Gilbert et al., 2000) and food safety
requirements within Regulation (EC) No. 178/2002 (General Food Law Regulation) (EC,
2002) (Table 1).
Table 1. Criteria for the interpretation of microbiology results, according to the HPA (PHLS) Guidelines for the microbiological quality of some ready-to-eat foods sampled at the point of sale
Satisfactory Acceptable Unsatisfactory Unacceptable/ Potentially Hazardous
E. coli /g <20 20 - <100 >100 N/Aa Salmonella in 25g Not Detected N/A N/A Detectedb
a, N/A, Not applicable b, Potentially injurious to health and/or unfit for human consumption (contravenes Article 14 Food Safety Requirements of Regulation (EC) No.178/2002 (the General Food Law Regulation)
Exclusion of Inappropriate Nut Samples
A further 41 samples of salted, flavoured or yoghurt coated nuts that were collected and
examined as part of this study but were not included in the final analysis of results as they
did not fit the study criteria.
Statistical Analysis
Descriptive and statistical analysis of the data was undertaken using Microsoft Excel.
Relative proportions were compared using the Chi squared test (χ2) and Fisher’s Exact Test.
A probability value of less than 5% was defined as significant.
Results
Prevalence of Salmonella spp. and Escherichia coli Salmonella spp. were detected in 0.1% (3) of 2,886 edible nut kernel samples, which were of
unacceptable microbiological quality. Escherichia coli was present in 0.8% (23) samples, of
which one sample (0.03%) was of unsatisfactory microbiological quality due to an E. coli
6
level of 150/g, a further five samples (0.2%) were of acceptable quality, and the remainder
(99.7%) were of satisfactory quality.
Details of the edible nut kernels contaminated with Salmonella and E. coli are as follows:
• S. Senftenberg and S. Tennessee were detected from two pre-packed samples of
Brazil nuts and S. Anatum from a pre-packed mixed nuts sample (mix: almonds,
brazils, cashews, peanuts, walnuts) (Table 2) indicating a risk to health.
o Salmonella was enumerated in the three samples. The Most Probable
Number was <0.01 to 0.23 /g (Table 2).
• All three Salmonella isolates were sensitive to all antimicrobial agents tested except
S. Anatum, which was resistant to tetracycline.
• E. coli at unsatisfactory levels (≥100/g) was present in another sample of pre-packed
Brazils (0.2%) (Table 2).
• E. coli was found at lower levels (range: 3.6 – 43/g) in additional samples of Brazils
(1.9%), macadamia (1.5%), pistachios (1.1%), walnuts (0.7%), peanuts (0.7%),
hazels (0.5%), cashews (0.4%), and almonds (0.3%) (Table 3).
• Of the single types of nuts sampled, Brazils were the most contaminated nut kernel
with regards to Salmonella (0.4%, p=0.0103) and E. coli (2.1%, p=0.0009) (Table 3).
Table 2. Details of Salmonella serotypes and E. coli (≥100/g) isolated from edible nut kernels from retail premises Type of shelled nut
Packaging Country of origin
Best before date
Date sampled
Salmonella serotype
Salmonella /g
E. coli/g
Brazils Pre-packed Not known
17/11/2009 09/12/2008 Senftenberg 0.23 <3
Brazils Pre-packed Not known
17/11/2009 16/12/2008 Senftenberg, Tennessee
0.09 <3
Mixeda Pre-packed Not known
30/08/2009
04/12/2008
Anatum <0.01 <3
Brazils Pre-packed Not known
19/11/2009 12/03/2009 Not detected - 150
a, Almonds, brazils, cashews, peanuts, walnuts
Although there is no direct evidence that these contaminated Brazils and mixed
kernels were responsible for any cases of human illness, during the period of the study two
of these subtypes were reported in cases of human infection in England and Wales: S.
Tennessee (26), S. Senftenberg (10 cases).
Details of edible nut kernels examined
The varieties of edible nut kernels sampled in the study are presented in Table 3. A greater
proportion of single types were sampled (88.6%), of which most were Brazils (18.4%),
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cashews (18.0%), walnuts (17.2%), and almonds (14.0%). Most of the nut kernels sampled
were whole (68.7%), halved/broken (18.1%), or a mix of whole and halved kernels (13.2%).
Edible nut kernels sampled were produced in 30 countries with most produced in the USA
(10.3%) (Table 4).
Of the edible nut kernels sampled, 94.0% were pre-packed (Figure 1) and 12.2%
were labelled as organic. Of the samples collected from open displays, 87.3% of the displays
had scoops to serve nuts, and of these 55.6% were used for individual types of nut kernels.
The premises types visited in the study to collect samples of edible nut kernels are
presented in Figure 2. Most nut kernels were sampled from either supermarkets (44.4%) or
health food shops (31.2%).
Table 3. Edible nut kernel types sampled in relation to presence of Salmonella and E. coli Variety of nut No. samples
n=2886 (%) No. samples Salmonella detected (%)
No. samples E. coli detected (%)
Single type 2557 (88.6) Almonds 359 (14.0) 0 1 (0.3) Brazils 469 (18.4) 2 (0.4) 10 (2.1) Cashews 459 (18.0) 0 2 (0.4) Hazels 195 (7.6) 0 1 (0.5) Macadamia 65 (2.5) 0 1 (1.5) Peanuts 148 (5.8) 0 1 (0.7) Pecans 151 (5.9) 0 0 Pine nuts 76 (3.0) 0 0 Pistachiosa 184 (7.2) 0 2 (1.1) Walnuts 441 (17.2) 0 3 (0.7) Other (Chestnuts,soya nuts) 10 (0.4) 0 0 Mixed kernel typesb 329 (11.4) 2 kernel types 6 (1.8) 0 0 3 kernel types 27 (8.2) 0 0 4 kernel types 131 (39.8) 0 0 5 kernel types 105 (31.9) 1 (0.9) 0 >5 kernel types 60 (18.2) 0 2 (3.3) a, Pistachios: kernels only (73); with shells (111). b, mixed types comprised combinations of single types listed in the table
8
Table 4. Country of origin of edible nut kernels Country of origin No. samples
n= 2886 (%) Australia 25 (0.9) Bolivia 209 (7.2) Brazil 85 (2.9) Chile 9 (0.3) China 223 (7.7) France 6 (0.2) Germany 8 (0.3) India 142 (4.9) Iran 46 (1.6) Italy 71 (2.5) Republic of Moldova 7 (0.2) South Africa 44 (1.5) South America - Amazonian rainforest 8 (0.3) Spain 26 (0.9) Sri Lanka 8 (0.3) Turkey 105 (3.6) UK 81 (2.8) USA 298 (10.3) Vietnam 95 (3.3) Produce of >1 country (countries not specified) 254 (8.8) Other a 27 (0.9) Not known (No details available) 1109 (38.4) a Channel Islands, El Salvador, Kashmir, Lebanon, Mexico, Netherlands, Nicaragua, Nigeria, Pakistan, Peru, Zambia
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Discussion Overall Salmonella spp. were not detected in the vast majority (99.0%; 2883/2886) of edible
nut kernels sampled. However, two samples of Brazil kernels and a mixed kernels sample
were found to be contaminated with Salmonella spp.; this is unacceptable. Ready-to-eat
foods contaminated with Salmonella spp. are unsafe. They are considered to be injurious to
health and/or unfit for human consumption and they therefore contravene the food safety
requirements (Article 14) of Regulation (EC) No.178/2002 (EC, 2002). The UK Food
Standards Agency was immediately informed, the affected batches were recalled and full
investigations undertaken (FSA 2008b, 2008c).
Levels of Salmonella enumerated from the three contaminated nut samples in this
study were low (<0.01 – 0.23/g). This is a similar finding to that found in a recent study of
edible dried seeds in the UK where Salmonella counts were low (<0.1 to 0.2 /g) (Willis et al.,
2009). Assuming an even distribution of Salmonella in a food, low levels of contamination as
shown in one of the samples tested here (e.g. <0.01/g) are unlikely to be detected in a 25g
test portion from a sample. Danyluk et al. (2006; 2007) has reported similar concentrations
of Salmonella from random samples of almonds arriving at processing facilities in California
from 2002 to 2004 (<0.01 to 0.03/g) and also from almonds recalled during the 2000 to 2001
outbreak of S. Enteritidis phage type 30 in the USA (0.06 to 0.09/g). Similarly, low numbers
(<0.03 to ~2/g) of salmonellae in peanuts in shell have been reported to cause an
international outbreak of salmonellosis in Australia, Canada, and the UK (Kirk et al., 2004).
This indicates that even low doses of Salmonella in these types of product may lead to
infection.
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Of the single kernel types sampled, only Brazils were contaminated with Salmonella
(0.4%). Significantly, Brazils also had the highest rate of E. coli contamination (2.1%),
including a sample with unsatisfactory levels (≥100/g). Salmonella has been previously
reported in Brazils (Freire and Oxford 2002) and also in chocolate coated Brazil nuts
produced in the UK where the company indicated that the contamination was most likely to
have come from a batch of Brazil nuts. However, the actual source of contamination was
not categorically identified (Anon, 2007). Brazils are still mainly collected directly from wild
trees in the forests of the Amazon basin and may lie on the forest floor for weeks before they
are harvested during the rainy season. This can allow extensive fungal and bacterial growth
to occur (Wareing et al., 2000). Reducing the time that these nuts remain on the ground too
long would mitigate against the risk of microbial contamination. Contamination may
potentially also occur after shelling and processing and during subsequent storage and
handling.
The use of E. coli as a feacal indicator organism is based on the concept that its
detection in food or water samples indirectly provides evidence that the sample has been
contaminated with faecal material and that pathogenic organisms may also be present
(Roberts and Greenwood, 2003). E. coli was present in seven different nut kernel types and
at an unsatisfactory level (≥100/g) in one sample of Brazil nuts. The use of E. coli as an
indicator organism in edible nut kernels and dried seeds has been recently challenged by a
number of investigators (Danyluk et al., 2007; Eglezos et al., 2008; Willis et al., 2009),
however no suitable substitute has been identified. The findings from the present study
corroborates with this view in that there was no significant association between presence of
E. coli and the detection of Salmonella in edible nut kernels. However as discussed above,
the Salmonella may be present at low levels and will consequently be unlikely to be detected
in a 25g test portion of the sample.
The prevalence of Salmonella in edible nut kernels, i.e. a finished product, surveyed
in this study on the UK retail market is low but nonetheless is unacceptable. The
international outbreak of salmonellosis in 2001 (Kirk et al. 2004) and the recent large
Salmonella outbreaks linked to almonds and peanut products in the US during 2008 (CDC
2004; 2009a) demonstrates that major health problems can arise from consumption of
contaminated edible nuts if production processes and/or hygiene practices break down. It
follows that the need for a sound approach to food safety management cannot be
overemphasized. Control measures to prevent bacterial cross-contamination of raw and
processed nuts require procedures for maintaining the hygienic quality of the processing
environment and equipment (Codex, 1972; EC, 2004). Application of good agricultural,
manufacturing and storage practices together with the hazard analysis and critical control
11
points (HACCP) system that encompass all stages of production, processing and distribution
will help ensure the microbial safety of edible nut kernels.
Acknowledgements The authors would like to thank all the staff in the Environmental Health Departments
throughout the UK who collected samples for this study, and the staff in HPA, HPA
collaborating laboratories and all other Official Control laboratories who performed the
microbiological examinations. Thanks are extended to LGP, HPA Centre for Infections for
typing Salmonella isolates, and Gemma Cantelo at LACORS for co-ordinating the
participation of Environmental Health Officers and advice from the LACORS Food
Examination and Food Hygiene Focus Groups, to the HPA Regional Food, Water and
Environmental Co-coordinators Forum for their contribution to the development and
implementation of this study, and to Lynn Cree (Health Protection Scotland) for providing
data from Scotland.
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Annex 1. Participating Laboratories and Local Authority Food Liaison Groups and number of samples Table 1a. Participating HPA and HPA Collaborating Laboratories and number of samples
HPA Region HPA/HPA Collaborating Laboratory Number of Samples East Chelmsford 247
Norwich 102 East Midlands Leicester 112
Lincoln 58 London London FWEM1 142 South East Ashford 145
Haywards Heath 65 WEMS2 380
North East Newcastle 246 North West Carlisle 52
Chester 76 Preston 442
South West Bristol 119 Plymouth 1 Truro 38
West Midlands Birmingham 260 Stoke on Trent 58 Hereford 8
Yorkshire & the Humber Sheffield 129 Total 2680
1 London Food, Water & Environmental Microbiology Services Laboratory 2 Wessex Environmental Microbiology Services
Table 1b. Other participating Official Food Control Laboratories in Wales, Scotland, and Northern Ireland and number of samples examined
Country Laboratory Number of Samples
Wales NPHS1 Wales-Bangor 22 NPHS Wales-Cardiff 26 NPHS Wales-Rhyl 19 Ireland Belfast City Hospital 58 Scotland Aberdeen City Council Public Analysts 16 Aberdeen Royal Infirmary 6 Edinburgh Analytical & Scientific Services 16 Glasgow Scientific Services 43 Total 206 1National Public Health Service - Wales
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Table II: Participating Food Safety Liaison Groups and number of samples Local Authority Food Liaison Group Number of Samples Berkshire 86 Buckinghamshire 21 Cambridgeshire 35 Cheshire 97 Cornwall 38 Cumbria 52 Derbyshire 69 Devon 15 Dorset 24 Durham 48 East Sussex 58 Essex 176 Gloucestershire 28 LFCG1 Greater London NE Sector 36 LFCG Greater London NW Sector 16 LFCG Greater London SE Sector 28 LFCG Greater London SW Sector 21 Greater Manchester 145 Hampshire & Isle of Wight 153 Hereford & Worcester 29 Hertfordshire & Bedfordshire 20 Kent 93 Lancashire 169 Leicestershire 112 Lincolnshire 19 Merseyside 107 North Yorkshire 12 Northamptonshire 106 Northern Ireland Food Group2 58 Norfolk 65 Nottinghamshire 35 Northumberland 18 Oxfordshire 48 Scottish Food Enforcement Liaison Committee3 81 Shropshire 23 Somerset 34 South West Yorkshire 64 Staffordshire 35 Suffolk 64 Surrey 65 Tees Valley 111 Tyne & Wear 57 Wales-North 41 Wales-South East 26 Warwickshire 43 West Midlands 99 West of England 43 West Sussex 45 Wiltshire 18 Total 2886
1 London Food Co-ordinating Group 2 Northern Ireland Food Group consists of Eastern, Northern, Southern & Western Groups 3 SFELG consists of Central Scotland, Lothian & Scottish Borders, North Scotland, East of Scotland and West of Scotland
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Annex 2
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