Current perspectives on the microbiological safety of fresh produce

Foodborne illness associated with fresh produce

Kevin Allen1 | Pascal Delaquis2*

Analysis of recent epidemiological data reveals that sporadic infections and full-blown outbreaks associated with the consumption of fresh fruits and vegetables contaminated with viral, bacterial or protozoan pathogens are occurring with increasing frequency in Western countries1. Some commodities are now recognized as important vehicles for the transmission of foodborne pathogens. For example, leafy green vegetables are a leading cause of infections with Escherichia coli O157:H72. Other commodities not previously associated with the dissemination of microbiological hazards, such as tomatoes and melons, have caused large outbreaks leading to serious threats to public health, loss of consumer confidence and substantial economic disruption. Several factors are believed responsible for this significant shift in the causality of foodborne illness, including increasing intake and variety of fresh fruits and vegetables in the diet, changes in primary production systems and agricultural practices, declining health of the agricultural environment, rapid expansion of the minimally processed (fresh-cut) sector and the growing complexity and length of supply and distribution chains. Producers, processors, wholesale distributors, retailers and regulatory agencies have responded vigorously to consumer concerns about the microbiological safety of fresh produce. Strategies for the control of microbiological contamination are increasingly deployed at ostensibly vulnerable stages along the production-to-consumption chain in conjunction with quality control or surveillance programs on regional or national scales to verify their performance. Such measures clearly alleviate risks to consumers. However, persistent reports of illness hint at weaknesses in current strategies for the control of foodborne pathogens in fresh produce.

Deficiencies in current strategies for the enhancement of fresh produce safety
Effective disinfection treatments could clearly eliminate food safety risks before fresh fruits and vegetables reach consumers. Although irradiation can reliably inactivate human pathogens in fresh produce, examples of successful commercial applications are scarce. Several technical, economic and socio-cultural factors have hindered uptake of irradiation technology by the food industry4. Consumer unwillingness to purchase irradiated food, whether a false perception or not, is an intangible risk that few food companies are either able or willing to assume. None of the alternative chemical or physical disinfection approaches proposed to date can deliver the antimicrobial efficacy or retention of eating quality achieved with irradiation. In the absence of an effective “kill step” the prevention of contamination and, where bacterial pathogens are concerned, reduction of opportunities for growth remain the focus of mitigation measures. The principles and approach inherent to Hazard Analysis Critical Control Point (HACCP) are increasingly applied to fresh produce production, processing and distribution systems to achieve these objectives. Science-based HACCP programs are developed through the recognition, quantification, assessment and ranking of risks associated with potential hazards to identify critical control points (CCPs) at specific stages along the production-to-consumption chain. The safety of many foods derived from well-characterized processing systems is ensured through the application of reliable HACCP programs, notably where inputs can be stringently controlled or where an effective kill step is applied. In contrast, the principles of HACCP are not easily adapted to the development of food safety programs for fresh produce. Factors that influence the fate of human pathogens are rarely constant due to the inherent complexity, variability and unpredictability of fresh produce chains. In addition, critical gaps in knowledge or the scarcity of relevant data often hinder the recognition of hazards, the assessment of implied risks or their ranking to identify and prioritize CCPs. Strategic research on the origin, characteristics, distribution and fate of human pathogens in fresh produce chains is clearly needed address these deficiencies.

Selected critical knowledge gaps and research needs
Undesirable microorganisms may enter fresh produce at many stages before and after harvest. Potential sources of contamination in relatively enclosed postharvest handling, processing and distribution operations are generally recognizable and controllable. In contrast, most production systems are open and subject to frequent known or latent microbiological risks that are difficult to rank and control. Here the microbiological quality of irrigation water stands out as an example of a challenge to the assessment and ranking of risks needed for the identification of CCPs. Natural irrigation water supplies such as rivers, lakes or reservoirs designed for the purpose are subject to contamination with variable and often unpredictable sources of microorganisms, including foodborne pathogens. Given that large volumes may be applied repeatedly to growing crops, irrigation water could introduce significant risks, specifically where pollution by animal or human wastes cannot be completely prevented. Reports from many parts of the world indicate that foodborne pathogens are often detected in supplies used for irrigation, albeit at very low concentrations. Unfortunately, the risks implied by very low numbers of foodborne pathogens applied to crops over the course of a production cycle are difficult to measure. Despite this uncertainty irrigation water quality is often considered a CCP requiring monitoring and control. Monitoring is currently expensive given the number of analyses required to ensure the performance of a testing program. Rapid, low cost methods or technologies for the detection of foodborne pathogens in water are urgently needed to improve the scope and validity of irrigation water quality monitoring. Where control is required producers are faced with serious challenges given the increasing scarcity of alternative natural supply options or lack of access to treated water in remote agricultural areas. Field deployable water treatment systems that can accommodate the volumes required for crop irrigation purposes would clearly contribute significantly to the reduction of risks associated with the microbiological quality of irrigation water.

Fresh fruits and vegetables are increasingly delivered to end-users in a fresh-cut format. Water containing an antimicrobial agent (chlorine based compounds, peroxyacetic acid, ozone or hydrogen peroxide) is routinely used to wash either the whole plant or cut tissues before packaging. Washing in sanitizer is widely considered a CCP as some of the microorganisms associated with produce surfaces may be inactivated by the treatment. Properly applied sanitizers can prevent cross-contamination during the wash step but their efficacy against surface-bound contaminants is limited and the tolerances which signal the need for corrective action for this CCP are narrow. Microorganisms located within recessed or damaged plant tissues are believed to remain protected from the effects of sanitizers. Attempts to improve the antimicrobial efficacy of washes using other chemicals, either alone or in combination with emulsifiers or ultrasound, have met with little success. Alternative physical treatments such as ultraviolet light, high powered pulsed light, cold plasma or application of antimicrobials in the gas phase are more likely to overcome the limitations inherent to sanitizing solutions and enhance the destruction of microorganisms on plant surfaces. All are the subject of considerable research at the present time.

Bacterial pathogens including Salmonella spp., Escherichia coli O157:H7 or Listeria monocytogenes are capable of growth in a range of fresh-cut products including leafy vegetables, apple slices or melon cubes. Since current processing schemes cannot ensure complete removal of contaminants, the maintenance of low temperature remains the only barrier to bacterial proliferation during distribution. Recent investigations have shown that temperature can fluctuate substantially in commercial distribution chains. An integrated study of the fresh-cut lettuce distribution chain in Canada showed that temperatures above the minimum required for growth of the pathogen Escherichia coli O157:H7 can occur during transportation between storage at processing plants, distribution centres and retail outlets3. However, the risk implied by disruptions in temperature control during the distribution of fresh produce remains difficult to estimate due to the limited amount of available data at this juncture. In addition, the influence of consumer practices on the risk of pathogen transfer or growth remains highly speculative due to the dearth of studies on food handling behaviour in the home.

Future prospects
Accurate assessments of risks along integrated fresh produce chains using conventional scientific approaches would require inoculation of products with foodborne pathogens to measure pathogen survival or growth at each stage. Because biosafety issues preclude experimentation with human pathogens in a commercial setting, mathematical modeling using laboratory-derived data is increasingly used to predict pathogen behaviour at different stages including production5, processing6, storage of fresh-cut products7 and in distribution chains for fresh produce8. The capacity to predict risks associated with individual stages paves the way for simulation of pathogen behaviour in complete chains and increasingly accurate ranking of risks for identification of CCPs. These advances will undoubtedly lead to the development of more effective HACCP programs and guide the development of improved control strategies focused on control of key microbiological hazards in fresh produce.

[1] Lynch, M.F. et al. (2009). Epidemiology and Infection,137:307.
[2] Berger, C.N. et al. (2010). Environmental Microbiology, 12:2385.
[3] McKellar, R.C. et al. (2012). Foodborne Pathogens and Disease, 9:239.
[4] Farkas, J., & Moh´acsi-Farkas, C. (2011). Trends in Science and Technology, 22:121.
[5] Bezanson, G. et al. (2012). Journal of Food Protection, 75:480.
[6] Pérez Rodríguez, F. et al. (2011). Food Microbiology, 8:141.
[7] McKellar, R. & Delaquis, P. (2011). International Journal of Food Microbiology, 51:7.
[8] McKellar, R.C. et al. (2014). Food Control, 35:192.

1 Faculty of Land and Food Systems, University of British Columbia,Vancouver, BC, Canada
2 Agriculture and Agri-Food Canada, Pacific Agri-Food Research Centre, Summerland, BC, Canada
(*Corresponding author: E-mail:

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