Zoonotic pathogens are microorganisms transmitted by animals, which cause disease and illness in humans. Many of them are foodborne and are commonly associated with farmed animals, or less frequently with wildlife. However, some pathogens are also transmitted into the food-chain indirectly from animals onto plants, via faecal contamination of water used for irrigation or via the soil where the plants grow. If the plants are destined for consumption, e.g., fruit and vegetable crops that are normally consumed raw or minimally processed, this can become a foodborne hazard.

Surprisingly though, there is still a misconception that plants play only a minor role in zoonoses survival and spread, even though fresh-produce accounts for similar numbers of foodborne outbreaks as meat or dairy. At SEFARI our researchers contribute to work in this area and are part of only a relatively small number of researchers in the UK & Ireland who do. In this blog, Dr Nicola Holden discusses how SEFARI research fits into this complex issue, outlines the key risk factors (illustrated with examples) and identifies what questions still need to be addressed.

Introduction:

SEFARI work has shown how zoonotic bacterial pathogens colonise crop plants [see: ‘Disease Threats in the Environment’ and ‘Animal Epidemiology’], and the risks involved [see: ‘Food Safety’]. This work has uncovered some of the bacterial genes involved in plant colonisation, examined how colonisation patterns differ between different species of crop plant, and shed new light on plant and soil bacteria that are closely related to the pathogens.

Bringing together our research with other relevant information, I recently (February 2021) presented findings to a joint working group for Animal & Plant Health (Defra, UKRI, APHA, RESAS) to highlight the key issues with relation to crops and the transmission of zoonotic pathogens. By working together, we want to extend our collective understanding of the issues and establish what action is still needed. The points I raised at the meeting are summarised here:

Headline facts:

• Between a third and a half of all foodborne illnesses are attributed to plant-based foodstuffs (produce) [Refs: 1,2,3].
• Any plant types can be contaminated, from salad vegetables to dried nuts & seeds [Ref: 4].
• Many zoonotic bacterial pathogens, including the most notorious (e.g., Shigatoxigenic Escherichia coli or STEC, Salmonella) can grow and establish as part of the plant’s microbial community [Ref: 4].
• The UK estimate the social and economic cost of all foodborne disease is ~£9.1bn per year (based on 2018 cases) [Ref: 5]. Separate plant-derived zoonoses figures are not available for the UK, but in the USA ~46 % of foodborne outbreaks are attributed to produce, and in Europe and Asia ~30% and ~46% of STEC cases, respectively, are from produce [Refs: 2,5].
• Some zoonotic pathogens can colonise crop plants for the complete plant growth cycle, e.g., Salmonella Typhimurium on tomato [Ref: 6].    

Which pathogens are mainly spread by plants?

• Foodborne pathogens including bacteria, virus and parasites. Viruses and parasites are transmitted passively since they require human / animal hosts for proliferation, whereas most bacterial pathogens can proliferate on plants directly, and use them as alternative hosts.
• The zoonotic pathogens include (STEC), non-typhoidal Salmonella enterica, Yersinia enterocolitica, while Norovirus, Listeria monocytogenes, Cryptosporidium, Shigella species are also transmitted by plants.

Which plants are involved?

• Ready-to-eat crops that are eaten raw or minimally processed, including leafy greens, salad alliums and celery, fruit, sprouted seeds and microgreens.
• Very young plants (sprouts, microgreens) with immature immune systems, are propagated under favourable conditions for pathogen growth.
• Low water-content products, e.g., seeds, nuts, ground herbs and spices are also key sources, especially for pathogens like S. enterica that switch to a different physiological state allowing them to persist for extremely long periods under these conditions [Ref: 7].

Sustainable food production and the economic cost of plant-associated zoonotic pathogens:

• Intensification in livestock and crop production increases the likelihood of cross-contamination from farmed animal sources (manure, contaminated irrigation water), hence increases the risk of zoonotic diseases via plants. For a recent example of SEFARI research see: ‘Protecting water catchments from zoonotic Cryptosporidium parasites’.
• Further pressures on marginal land have increased contact with wild animals and therefore the potential for increased risk to crop production from cross-contamination.
• Climatic change is likely to increase water-borne transmission, e.g., from flooding/run-off. It also means longer seasons for crop production in temperate zones.
• Emerging agricultural technologies that are still in development have unknown levels of risks e.g. vertical farming.
• Lessons need to be learnt from previous outbreaks, e.g., legislation introduced for sprouted seed production after large-scale 2011 outbreak.
• Other relevant SEFARI food research examples include: ‘Scotland’s Dinner Plate 2050’, ‘What we eat, and meeting our climate change commitments’, ‘Increasing uptake of best practice’ and ‘Improving Primary Produce’.

Examples of recent outbreaks:

• International: May 2011, 4075 cases (50 fatalities) STEC O104:H4, associated with fenugreek seeds from Egypt, cultivated & distributed from Germany. 
• UK: Sept 2015, 38 cases STEC O157:H7, associated with UK-produced lettuce.
• UK: July 2016, 161 cases (2 fatalities, 62 hospitalisations) STEC O157:H7, linked with rocket / mixed salad leaves.
• UK: Aug 2018, 147 cases Salmonella enterica serovar Agnona, associated with cucumbers imported from Spain.
• UK recall: Summer 2020, multiple products contained Brazil nuts due to S. enterica contamination.
• Sweden: March 2021, 53 cases Yersinia enterocolitica linked to lettuce, which may relate to recent Y. enterocolitica outbreak in Norway in Dec 2020 (10 cases) linked to salad.
• USA: March 2021, 22 cases (1 fatality) STEC O157:H7, identified from Romaine lettuce. The same genetic strain was responsible for repeated outbreaks in USA & Canada since 2018.

Questions that still need addressing:

• Is the observed increase in produce-associated outbreaks of zoonotic pathogens (e.g., STEC, Salmonella) due to more transmission events from farmed animals to produce, or are the pathogens becoming more common or habituated to crops and soils?
• How does the passage of zoonoses through plants and soil affect their pathogenicity, i.e. do they cause similar levels of disease as if they were transmitted directly from animals?
• What are the implications for antimicrobial resistance of zoonotic pathogens in soil / on plants? 
• What drives the emergence of ‘new’ pathogens or novel hybrids (e.g., STEC O104:H4) transmitted by crop plants?
• Is there a growing risk from opportunistic pathogens transmitted by crop plants?
• What are the plant-dependent mechanisms that enable zoonotic pathogens to live on plants and are some varieties of produce at more risk or harbouring them?

Recommendations for future work:

• The work requires collaboration between bacteriology, food safety, plant-microbe interaction, animal health, zoonoses. Research groups that have the potential to work in this area and should be encouraged to do so (e.g., Control of Human Pathogenic Micro-organisms in Plant Production Systems, SEFARI, etc.).
• Include the role of plants in any zoonoses-related research projects.
• Encourage multidisciplinary funding applications to bring in new skills to strengthen this area of research, e.g., within the One Health agenda.   
• Make use of existing networks and consortia outside the immediate area of zoonoses, e.g., EPIC, Plant Health Centre, CREW, ClimateXChange, FSS and Public Health Scotland.

Concluding remarks:

In the UK, we enjoy world-renowned standards of food safety that keep the number of foodborne illnesses and outbreaks from zoonotic pathogens relatively low. However, and as for any preventable disease, we can never let our guard down and need to keep up to date with new developments, and what their implications for human health are. Knowledge exchange between different research groups is a key aspect in helping us all towards common goals. For me, one of the most rewarding aspects has been working with others outside my own research area in order to find solutions. Fresh produce is a vital part of a healthy diet, and at SEFARI we will continue to collect scientific evidence that underpins risk management strategies and helps to keep our food safe.

Dr Nicola Holden (SRUC, James Hutton Institute).

References:

1 Bennett, S., Sodha, S., Ayers, T., Lynch, M., Gould, L., & Tauxe, R. (2018). ‘Produce-associated foodborne disease outbreaks, USA, 1998–2013’. Epidemiology and Infection, 146(11), 1397-1406. Doi:10.1017/S0950268818001620.

2 Pires, S., Majowicz, S., Gill, A., & Devleesschauwer, B. (2019). ‘Global and regional source attribution of Shiga toxin-producing Escherichia coli infections using analysis of outbreak surveillance data’. Epidemiology and Infection, 147, 236. Doi:10.1017/S095026881900116X

3 Greig,J. D. & Ravel,A. (2009) ‘Analysis of foodborne outbreak data reported internationally for source attribution‘. International Journal of Food Microbiology, 130(2), 77-87. doi.org/10.1016/j.ijfoodmicro.2008.12.031.

4 Holden. N.J., Jackson, R.W. & Schikora, A. (2015) ‘Editorial on plants as alternative hosts for human and animal pathogens’. Frontiers in Microbiology, 6:397. Doi: 10.3389/fmicb.2015.00397.

5 Food Standards Agency (2020) ‘The Burden of Foodborne Disease in the UK 2018’. Available at: https://www.food.gov.uk/research/research-projects/the-burden-of-foodborne-disease-in-the-uk-2018.

6 Guo, X., Chen, J., Brackett, R. E. & Beuchat, L. R. (2001) ‘Survival of Salmonellae on and in Tomato Plants from the Time of Inoculation at Flowering and Early Stages of Fruit Development through Fruit Ripening’. Applied and Environmental Microbiology, Oct, 67(10) 4760-4764. Doi: 10.1128/AEM.67.10.4760-4764.2001.

7 Finn, S., Condell, O., McClure, P., Amézquita, A. & Fanning, S. (2013) ‘Mechanisms of survival, responses and sources of Salmonella in low-moisture environments’. Frontiers in Microbiology, 4, 331. Doi: 10.3389/fmicb.2013.00331.