Microbiological quality of vegan alternatives to dairy and meat products in England during 2022–3

Abstract

Aims

Plant-based alternatives to meat and dairy products have become increasingly popular in the UK. Despite a public perception that they have a relatively low microbiological risk, outbreaks of illness have been linked with these foods. This study aimed to assess the microbiological safety and quality of vegan alternatives to dairy and meat products available in England.

Methods and results

Samples were collected between September 2022 and March 2023 from retail, production, and catering premises, and tested for a range of bacterial pathogens and hygiene indicators using standard procedures. A total of 937 samples were tested, of which 92% were of a satisfactory microbiological quality, 3% were borderline, and 5% were unsatisfactory. Those interpreted as unsatisfactory were due to elevated counts of Enterobacteriaceae and Escherichia coli (indicators of poor hygiene) rather than pathogenic microorganisms. Listeria monocytogenes was present in five samples of tofu, all from the same producer (all at counts of <100 CFU g^–1), while other Listeria species were detected at counts of <20 CFU g^–1 in two burgers and two ‘vegan chicken’ products. The majority of samples did not have pH and water activity values that would significantly contribute to preventing microbial growth: 62.4% had pH > 5.0 and 82.4% had A_w > 0.94.

Conclusions

The majority of vegan products examined were of a satisfactory quality, but results demonstrate that microbiological control must be maintained using appropriate processing and storage temperatures, and application of a safe length of shelf life.

vegan, plant-based, microbiological quality, Bacillus cereus, coagulase-positive staphylococci, E. coli, Enterobacteriaceae, Listeria, Salmonella

Impact Statement

This study is one of the first to assess the hygiene and microbiological safety of vegan alternatives to meat and dairy products. While results were largely satisfactory, it is important that producers and retailers understand the appropriate control measures to maintain safety throughout shelf life.

Introduction

Plant-based foods consumed as alternatives to meat and dairy products have become increasingly popular in the UK in recent years. Consumers are choosing plant-based alternatives for environmental, lifestyle, and health reasons. A third of British meat eaters reported reducing their meat consumption in July 2018, and sales of meat-free foods grew by 40% between 2014 and 2019 (Mintel 2020). In 2019, it was reported that the UK had overtaken Germany as the nation with the highest number of new vegan food products launched (Mintel 2019).

While products of animal origin tend to be considered higher risk than plant-based products in terms of microbiological safety (Dewey-Mattia et al. 2018, Piglowski 2019), there have been reports of foodborne outbreaks associated with nuts (ECDC-EFSA 2020), seeds (EFSA 2011, Meinen et al. 2019), flour (Vasser et al. 2021), and other plant-based products (Farakos and Frank 2014). Da Silva Felicio et al. (2015) produced a risk ranking model for pathogens in ready to eat, non-processed foods of non-animal origin, which identified a strong risk for Shigella in fresh pods, legumes, and grains, and moderate risks for Salmonella in nuts and nut products as well as Shiga-toxin-producing Escherichia coli (STEC) and Staphylococcus aureus in fresh pods, legumes, and grains.

Vegan alternatives to milk of animal origin are commonly produced by soaking nuts, grains, or pulses in water, while cheese alternatives may be made by soaking nuts, with or without a subsequent fermentation stage. In 2021, a Brie-style cashew nut cheese caused an outbreak of Salmonella Duisburg, affecting 20 people in the USA (Lewis et al. 2023). An outbreak of listeriosis in France in 2022 was linked to nut-based cheese alternatives, and affected five people, including four pregnant women who delivered prematurely (Outbreak News Today 2023). An oat-based drink was linked with two reports of illness in 2022 (Food Safety News 2022) and Bacillus cereus was identified in the implicated product. Plant-based beverages (coconut, almond, or cashew) were observed to support the growth of Salmonella, Listeria monocytogenes, and Paenibacillus strains at a higher growth rate than in bovine milk (Bartula et al. 2023), although Bacillus subtilis grew equally fast in bovine milk and almond drink. The authors of this study concluded that plant-based beverages may present a significant risk for listeriosis and salmonellosis, and that recommendations for handling the products post-opening should be carefully considered.

Meat alternatives are formulated with a similar protein, fat, and moisture content to meat, and neutral pH levels, which provide suitable growth conditions for pathogenic and spoilage organisms. A study by Tóth et al. (2021) concluded that the raw materials used in meat analogues were more perishable than meat products. Microbes proliferated faster in samples containing meat alternatives, especially when the meals were cooled slowly.

Despite evidence of microbial contamination associated with these food types, production of plant-based vegan products is frequently seen as a low-risk process. The purpose of this study was to investigate the microbiological quality of vegan foods (with a focus on ready-to-eat products) collected from retail, production, and catering premises during 2022–3, and to assess whether physical characteristics such as pH and water activity may be sufficiently low to control the growth of bacterial pathogens during the shelf life of these products.

Materials and methods

Sample collection

Samples of plant-based alternatives to meat, fish, or dairy products were collected over the period from 1 September 2022 to 31 March 2023 by environmental health practitioners in accordance with the Food Standards Agency's Food Law Practice Guidance (Food Standards Agency 2023). Sampling officers were requested to focus particularly on ready-to-eat items that did not require further processing prior to consumption. Samples were transported in insulated containers with sufficient frozen ice packs to maintain a temperature between 2°C and 8°C. All samples were examined by one of the three UK Health Security Agency (UKHSA) Food, Water and Environmental Microbiology (FW&E) Laboratories in England located in London, Porton, or York. Microbiological testing commenced within 36 h of sampling.

Data were collected by local authority staff on each individual sample using a standardized questionnaire that included the type, name, and address of the business premises; date, time, and temperature of the sample at collection; a sample description and type of product; the use-by date for the consumer; country of origin; packaging type; and whether resampling had occurred in the same premises due to a previous poor microbiological result or because of physical observations of hygiene concerns in the businesses’ environments. The information from the questionnaire was recorded via the FW&E laboratory information management system (LIMS) and extracted into Excel spreadsheets. To reduce bias on the microbiological results from examination of these foods, products known to be associated with incidents of foodborne illness were not included in this survey.

Microbiological examination

Samples were examined using internationally recognized standard methods and using culture media supplied either by E & O Laboratories Ltd, Bonnybridge, UK, or by Thermo Fisher Scientific, Basingstoke, UK. Examinations comprised: detection of Salmonella spp. (ISO 6579:2017; all ISO standards available at https://iso.org) by pre-enrichment in Buffered Peptone Water followed by enrichment in Muller–Kauffman tetrathionate novobiocin and Rappaport-Vassiliades broths and subculture onto xylose lysine deoxycholate and brilliant green agars; detection and enumeration of Listeria spp., including L. monocytogenes (ISO 11290-1:2017 and 11290-2:2017) by enrichment in half Fraser followed by Fraser broth and subculture onto chromogenic Listeria and Oxford agars; enumeration of the B. cereus group (based on BS EN ISO 7932:2004;) using a surface inoculation technique on Mannitol egg yolk agar; enumeration of β-glucuronidase producing E. coli (based on BS ISO 16649-2:2001) using either a surface spread or a pour plate technique on tryptone bile agar; enumeration of coagulase-positive staphylococci (based on BS ISO 6888-1:2021) using a surface spread plate on Baird–Parker agar; enumeration of Enterobacteriaceae (using either BS ISO 21528-2:2017 or the TEMPO^® EB technique [(Biomerieux, Basingstoke, UK) (Owen et al. 2010)]; and enumeration of an aerobic colony count (ACC) by surface inoculation (based on BS EN ISO 4833-2:2013 + A1:2022). Single samples were collected for each product tested and all presence/absence tests were performed on 25 g aliquots.

The confirmation of identity of bacterial isolates was performed in each of the individual testing laboratories as outlined in the standard methods earlier. Microbiological results were interpreted as unsatisfactory, borderline, or satisfactory according to the guidelines for assessing the microbiological safety of ready-to-eat foods placed on the market (Health Protection Agency 2009). Regulation (EC) No. 2073/2005 (as amended) on microbiological criteria for foodstuffs (European Commission 2005) was also used to interpret L. monocytogenes results (Table 1).

Table 1.

Interpretive criteria for microbiological test results.^a

	Microbiological quality (CFU g–1)
Target	Satisfactory	Borderline	Unsatisfactory	Unacceptable/potentially hazardous
Salmonella	Not detected in 25 g	N/A	N/A	Detected in 25 g
L. monocytogenes	<10	10–100	N/A	>100
Listeria speciesb	<10	10–100	>100	N/A
E. coli	<20	20–100	>100	N/A
Enterobacteriaceae	<100	100–104	>104	N/A
B. cereus group	<103	103 to <105	>105	N/A

N/A: not applicable.

a

Health Protection Agency (2009) and European Commission (2005).

b

Not including L. monocytogenes.

For a sub-set of the samples, pH and water activity were also determined (for the first five months of the study, all samples were tested for pH and all non-liquid samples for water activity). The samples were first allowed to equilibrate to room temperature. For pH determination of solid food samples, a representative portion was taken and a pH electrode was placed either against a cut surface of the sample or into a homogenate of the sample. For liquid products, the pH electrode was placed directly into an aliquot of sample. Water activity was determined using the Novasina LabMaster water activity meter (Novatron Scientific Ltd, Horsham, UK) according to the manufacturer's instructions.

Characterisation of L. monocytogenes by whole genome sequencing

Cultures of L. monocytogenes were sent to the UKHSA Gastrointestinal Bacteria Reference Unit (GBRU) for confirmation and further characterisation by whole genome sequencing (WGS), as described previously (Chattaway et al. 2016, McLauchlin et al. 2021). Briefly, DNA from purified cultures of L. monocytogenes was obtained by automated extraction (QIAsymphony DSP DNA Kit, Qiagen, Manchester, UK) according to manufacturer's instructions. Genomic DNA was sequenced by the UKHSA Central Sequencing Laboratory: sample was prepared using Nextera XT (Illumina Inc, San Diego, USA) and sequenced using the Illumina HiSeq 2500 platform with 2 × 100 bp reads (Illumina, Inc.). Short reads were quality trimmed using Trimmomatic removing the sequence adaptor. Clonal complexes (CCs) were derived from WGS analysis and were assigned using Metric Oriented Sequence Typer (MOST) (Tewolde et al. 2016) in accordance with the designation of the Institut Pasteur International Multilocus sequence typing (MLST) database for L. monocytogenes (http://bigsdb.pasteur.fr/listeria/listeria.html). A core single-nucleotide polymorphism (SNP) alignment for each CC was generated using SnapperDB (Dallman et al. 2018). Pairwise comparisons of SNP distances were performed between cultures within similar CCs (Dallman et al. 2018). Isolates linked within a 5 SNP single-linkage cluster were considered to be part of the same point source with each culture having ≤5 SNPs difference with at least one other culture within that same cluster. Genomic data were stored in a customized database (Gastro Data Warehouse), and pairwise comparisons of SNP addresses were performed on isolates from vegan products and cultures from clinical cases, which occurred in the UK, as well as other isolates from food or the environment. Sequence data are available through https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA248549.

Statistical methods

Descriptive analysis of the data was undertaken by using Microsoft Excel (Microsoft Corporation, Redmond, WA, USA). Statistical analysis was carried out using Fisher's exact test (GraphPad Software). A probability value of <5% was defined as significant.

Results

Sample types and origins

Overall, 937 samples were collected by sampling officers from 92 local authorities in England. Of these, 414 (44%) were meat substitutes, 246 (26%) were vegan cheeses, 138 (15%) were plant-based milks, 112 (12%) were other dairy alternatives, 11 (1%) were fish alternatives, and 16 (2%) were other vegan items, including tofu, egg alternatives, and vegan desserts. Of the 937 samples, 841 (89.8%) were from retail, 88 (9.4%) were from producers , and 8 (0.9%) were from catering.

The majority of samples (746; 79.6%) were pre-packed in unopened packaging at the time of sampling (Table 2). A further 25 samples (2.7%) were described as being pre-packed, but packs were already opened at the point of sampling. A total of 90 samples (9.6%) were described as ‘loose’ (i.e. not pre-packed), and this information was not available for 76 samples (8.1%).

Table 2.

Microbiology results for vegan products categorized by type of product, packaging, and sampling setting.

Category of sample	Number of samples (%)	Number (%) of samples with specified result
		E. coli > 102 CFU g–1	B. cereus > 103 CFU g–1	Listeria species detected in 25 g		Enterobacteriaceae (CFU g–1)
				L. monocytogenes	Other spp.	<102	102–104	>104
Total samples	937	3 (0.3)	2 (0.2)	5 (0.5)	4 (0.4)*	869 (92.7)	30 (3.2)	38 (4.1)
Cheese alternatives	246 (26.3)	3 (1.2)	2 (0.8)	0	0	228 (92.7)	7 (2.8)	11 (4.5)
Milk alternatives	138 (14.7)	0	0	0	0	138 (100)	0	0
Other dairy alternatives	112 (12.0)	0	0	0	0	108 (96.4)	4 (3.6)	0
Fish alternatives	11 (1.2)	0	0	0	0	11 (100)	0	0
Meat alternatives	414 (44.2)	0	0	5 (1.2)	4 (1.0)	368 (88.9)	19 (4.6)	27 (6.5)
Other vegan foods	16 (1.7)	0	0	0	0	16 (100)	0	0
Packaging type
Loose	90 (9.6)	0	0	0	0	74 (82.2)	6 (6.5)	10 (11.1)
Pre-packed—open	25 (2.7)	0	0	0	2 (8.0)	21 (84.0)	4 (16.0)	0
Pre-packed—unopened	746 (79.6)	3 (0.4)	2 (0.3)	5 (0.7)	2 (0.3)	711 (95.3)	15 (2.0)	20 (2.7)
Not stated	76 (8.1)	0	0	0	0	63 (82.9)	5 (6.6)	8 (10.5)
Settings
Retailer	841 (89.8)	3 (0.4)	2 (0.2)	0	4 (0.5)	801 (95.2)	19 (2.3)	21 (2.5)
Producer	88 (9.4)	0	0	5 (5.7)	0	61 (69.3)	10 (11.4)	17 (19.3)
Caterer	8 (0.9)	0	0	0	0	7 (87.5)	1 (12.5)	0

*

Other Listeria species comprised two L. seeligeri, one L. innocua, and one L. welshimeri.

Results of microbiological testing

Results of microbiological testing for each of the target bacterial groups/parameters are shown in Table 3. Combining the results for all microbiological parameters, 866 (92%) were of a satisfactory microbiological quality, 27 (3%) were borderline, and 43 (5%) were unsatisfactory. The results interpreted as unsatisfactory were due to elevated counts of Enterobacteriaceae and E. coli (indicators of poor hygiene) rather than the presence of pathogenic microorganisms.

Table 3.

Percentage of samples of vegan products with satisfactory, borderline, or unsatisfactory microbiological quality for different target bacteria.

		Number (%) of samples
Target bacteria	Number of samples tested	Satisfactory	Borderline	Unsatisfactory
All targets	937	866 (92.4)	27 (2.9)	43 (4.6)
B. cereus	920	918 (99.9)	2 (0.2)	0
Enterobacteriaceae	937	869 (92.7)	30 (3.2)	38 (4.1)
E. coli	937	934 (99.7)	0	3 (0.3)
L. monocytogenes	937	934 (99.7)	3 (0.3)	0
Listeria species (other than L. monocytogenes)	937	937 (100)	0	0
Salmonella	927	927 (100)	0	0

ACC were relatively low (<10⁴ CFU g^–1) in 88% of samples, with a higher proportion of elevated counts seen in cheese (15% with ACC > 10⁴ CFU g^–1) and meat alternatives (16%) compared to milk (2%) and other products (5%) (Table 4). This difference was significant (Fisher's exact test: P < 0.002). Counts were also more likely to be elevated in those samples that were loose (unpackaged) or in open packages at the time of sampling (24% with ACC > 10⁴ CFU g^–1) compared to those that were in unopened packs (10.6%; Fisher's exact test: P = 0.0003; Table 4). A higher proportion of samples that were unpackaged or in opened packages also had borderline or unsatisfactory Enterobacteriaceae levels (17.4%) compared to those in unopened packs (4.7%; Fisher's exact test: P < 0.0001; Table 2).

Table 4.

Percentage of samples of vegan products with ACCs within the specified ranges.

		Number (%) of samples with ACC (CFU g–1) in specified range
Category of sample	Number of samples tested	<104	104 to <105	105 to <106	106 to <107	≥107
Cheese alternatives	245	207 (84.5)	9 (3.7)	10 (4.1)	5 (2.0)	14 (5.7)
Milk alternatives	136	133 (97.8)	2 (1.5)	0	1 (0.7)	0
Other dairy alternatives	112	103 (92.0)	4 (3.6)	0	0	5 (4.5)
Fish alternatives	11	10 (90.9)	0	1 (9.1)	0
Meat alternatives	412	344 (83.5)	23 (5.6)	18 (4.4)	11 (2.7)	16 (3.9)
Other vegan foods	16	16 (100)	0	0	0	0
Packaging type
Loose	90	67 (74.4)	11 (12.2)	5 (5.6)	3 (3.3)	4 (4.4)
Pre-packed—open	23	19 (82.6)	2 (8.7)	1 (4.3)	0	1 (4.3)
Pre-packed—unopened	744	665 (89.4)	22 (3.0)	20 (2.7)	9 (1.2)	28 (3.8)
Not stated	75	62 (82.7)	3 (4.0)	3 (4.0)	3 (4.0)	4 (5.3)

Salmonella was not detected in any samples, B. cereus was detected at borderline levels in two samples (Table 3), L. monocytogenes was present in five samples (all at counts of <100 CFU g^–1), and other Listeria species were detected in four samples (all at counts of <20 CFU g^–1). Of the samples in which L. monocytogenes was detected, two had Enterobacteriaceae counts of >10⁴ CFU g^–1 and three had counts between 10² and 10⁴ CFU g^–1.

The five samples in which L. monocytogenes was detected were all samples of tofu from a single producer. One organic natural tofu sample, collected from a retailer in January 2023, highlighted an initial problem (L. monocytogenes detected at a count of 20 CFU g^–1), which led to follow-up sampling directly from the producer on a further three occasions: five follow-up samples of organic natural tofu were taken from the producer in early February 2023, with L. monocytogenes detected in three (of which one was at a count of 20 CFU g^–1 and two were at <20 CFU g^–1); five samples of various tofu products (natural, smoked, marinated tofu, and tofu burgers) were taken in late February, all of which were negative for Listeria; and five more samples of different product types were taken in March 2023, of which L. monocytogenes was detected in one marinated tofu sample (20 CFU g^–1).

Samples in which other Listeria species were detected were all meat substitutes: two burger samples contained L. welshmeri and L. innocua, respectively, while two ‘chicken’ products both contained L. seeligeri.

Characterisation of L. monocytogenes

Isolates from the original tofu sample (collected in January 2023), two of the follow-up samples (February) and the final follow-up sample (March) were all of serotype 1/2a, ST37 with whole genome sequences showing that they were identical strains with 0 SNP difference between them. In contrast, the isolate from the third sample collected from the same production premises in February was of serotype 4, ST145, which was therefore unrelated to the 1/2a strain. Interrogation of the UKHSA database did not identify any isolates from cases of human illness that were closely related to these food isolates (at the <25 SNP level).

Determination of pH and water activity in vegan products

A total of 772 samples were tested for pH. Of these, 41 (5.3%) had a pH of <4.0; 108 (14.0%) had pH between 4.0 and 4.5; 141 (18.3%) had pH between 4.5 and 5.0; and the remainder (62.4%) had pH > 5.0. Water activity was determined for 500 samples. Of these, 7 samples (1.4%) had A_w < 0.9; 81 (16.2%) had A_w between 0.9 and 0.94; and 412 (82.4%) had A_w > 0.94.

The five tofu samples in which L. monocytogenes was detected gave pH values between 5.3 and 6.3, and for two of these samples where A_w was determined, the A_w was 0.97. A sample of Camembert-style cheese with a borderline level of B. cereus (2800 CFU g^–1) had pH 5.2 and A_w 0.95–neither of which would be sufficiently low to prevent the growth of B. cereus. The second sample with a borderline B. cereus level (8800 CFU g^–1) was a garlic and herb ‘soft cheese’ product, and this had pH 4.4, which is sufficiently low to control B. cereus growth during shelf life (A_w not determined for this product).

Discussion

This study is one of the first to assess the hygiene and microbiological safety of vegan alternatives to meat and dairy products. Products of non-animal origin are recognized as being associated with outbreaks of infection (EFSA 2013, Callejon et al. 2015, Bennett et al. 2018). There are multiple opportunities for microbial contamination of plant-based ingredients before, during, and after harvest as well as during processing and in retail, catering, and domestic environments. In addition, these products may be subject to further processes such as fermentation during production of the final product, which may introduce additional opportunities for pathogen growth. However, results from this study have demonstrated that the vast majority of plant-based alternatives to meat and dairy products, sampled at retail, catering, or production in England, were of a satisfactory microbiological quality.

The collection of appropriate samples for this study was dependent on environmental health practitioners across England selecting samples according to specified instructions. While instructions requested a focus on ready-to-eat products in particular, some samples did not appear to be ready to eat (e.g. ‘meat-free burgers’ might be expected to be heated prior to consumption). For these samples, interpretation according to the criteria in Table 1 may be excessively stringent, but even taking this into account, the proportion of unsatisfactory samples was low.

Interpretation of results as borderline or unsatisfactory included consideration of Enterobacteriaceae levels. These are a group of Gram-negative bacteria that may be naturally present in non-processed plant-based ingredients. While they are readily killed by heat processes, it may be normal to find these organisms in plant-based products that do not involve a heating stage during production. The majority of bacteria in this group are non-pathogenic, but their presence in cooked, ready-to-eat foods can be an indication of poor hygiene; moreover, these organisms can contribute to spoilage of foods, even at refrigeration temperatures. Therefore, for the purposes of this study, the criteria specified in Table 1 were used for the interpretation of Enterobacteriaceae results. On this basis, 3% of samples had a borderline level of Enterobacteriaceae and 4% had an unsatisfactory level. This may be a slightly overcautious interpretation where products have not undergone a heat process, but since information on production processes is not always available at the time of testing in the laboratory, a more cautious approach was considered to be appropriate. Moreover, a higher proportion of samples that were unpackaged or in opened packages at the time of sampling had borderline or unsatisfactory Enterobacteriaceae levels compared to those in unopened packs, indicating that poor hygiene/cross-contamination may explain at least some of the elevated levels of this group of bacteria.

The low ACCs in the majority of milk samples are likely to reflect the frequent use of ultra-heat treatments or other high-temperature processes on these products to achieve microbiological stability at ambient temperature during an extended shelf life. In contrast, a higher proportion of the meat and cheese-style products had elevated ACCs, which is consistent with lower cooking temperatures (or no cooking) and the use of fermentation processes during production of some of these products.

It is recognized that ingredients commonly used in vegan cheese and milk production, such as nuts, beans, and oats, may be frequently contaminated with spore-forming microorganisms, including B. cereus (Akbas and Ozdemir 2006, Kyrylenko et al. 2023). Nicholls et al. (2016) described an outbreak of B. cereus food poisoning amongst 182 children and 18 staff attending nurseries in the UK, and reported that the conditions used by the caterer to soak dried beans prior to cooking in one of the products supplied to the nurseries was likely to have allowed growth of B. cereus to sufficient levels to cause illness. Moreover, an outbreak of B. cereus food poisoning that affected 20 children in Norway was reported to be linked to the consumption of porridge (Food Safety News 2024). Production of plant-based dairy alternatives often involves a heat-treatment step, which would be expected to reduce bacterial numbers in the final product. However, spore-forming bacteria such as Bacillus and Clostridium species are more likely to survive the heat process. Control of Bacillus growth in such products may include maintaining a low pH and/or water activity, low storage temperature, and potentially modified atmosphere. Two samples of soft-style vegan cheese had borderline counts of B. cereus (>10³ CFU g^–1). One of these products had a pH level that would be low enough to minimize the growth of Bacillus, but for the other product, neither the pH nor the water activity was sufficiently low to control Bacillus growth. Therefore, storage at an appropriate refrigeration temperature (with or without modified atmosphere) and maintenance of an appropriate length of shelf life would be important to ensure the continued microbiological safety of these products.

Listeria monocytogenes was detected at low counts in five tofu products from the same producer over a 2-month period. According to microbiological criteria set out in EC 2073/2005 (as amended) (European Commission 2005), the detection of L. monocytogenes in a 25 g portion of ready-to-eat food is acceptable in any product that has left the control of the manufacturer, as long as the count does not exceed 100 CFU g^–1 during shelf life. However, at the end of the manufacturing process, presence of L. monocytogenes, even at counts of <100 CFU g^–1, is unsatisfactory unless the shelf life is less than 5 days or the pH and water activity are low enough to control growth (i.e. pH ≤ 4.4 or A_w ≤ 0.92, or a combination of pH ≤ 5.0 and A_w ≤ 0.94). While tofu is generally subjected to further cooking prior to consumption (so would not normally be considered ready to eat), there are recipes available that use uncooked or lightly cooked tofu as ingredients. Therefore, while the risk of L. monocytogenes infection from these tofu products is likely to be low, it is undesirable for L. monocytogenes to be present, particularly given the high (i.e. non-inhibitory) pH and A_w values in these product types. Other Listeria species were detected in four different meat-substitute products. These species are not pathogenic, but do indicate that the conditions during production and/or post-production storage and handling have allowed Listeria to be introduced and to survive, and therefore highlight a potential risk of L. monocytogenes presence in these product types.

Results from this study indicate that pH and water activity are rarely sufficiently low to control pathogen growth (only 37% of those tested had pH < 5.0 and 18% had A_w < 0.94). Therefore, these physical parameters are unlikely to have a significant impact on the safety of products during shelf life, and microbiological control must depend on appropriate processing and storage temperatures, and determination of a safe length of shelf life for the majority of products of this type.

While this study provides reassuring evidence that plant-based alternatives to meat and dairy products consumed in England are generally of low microbiological risk, it is important that producers and retailers maintain an awareness of relevant risks and reliable controls.

Acknowledgements

The authors would like to thank colleagues in local authorities for sampling and investigations, and staff in the UKHSA laboratories for testing and providing information involved in this survey. No ethical approval was required..

Author contributions

Caroline Willis (Writing – original draft), Catherine Startin (Investigation, Writing – original draft), Frieda Jorgensen (Methodology, Writing – review & editing), Lorraine Sadler-Reeves (Methodology, Project administration), Heather Aird (Investigation, Methodology), Sandra Lai (Investigation), and Corinne Amar (Investigation, Writing – review & editing)

Conflict of interest

None declared..

Funding

None declared.

Data availability

The data underlying this article are available in the article.