Microbial risks during indoor leafy green production: Current knowledge and future research needs

Food crop production in controlled environments is an increasingly important sector of U.S. and global agriculture. Controlled environment agriculture (CEA) takes advantage of technologies and automation to modify production climates, shield crops from biotic and abiotic stresses, and optimize environmental factors that maximize plant yield and quality. Although CEA helps exclude pests and diseases from produce, pathogen issues can still occur in these operations. As the volume of information on the microbial risks within CEA grows, there is a need to synthesize the state of the science to identify evidence-based best practices as well as future research needs to enhance the safety of CEA-grown produce, specifically leafy greens. To address this need, we will identify both best practices and research gaps in the peer-reviewed literature, technical abstracts, and grey literature. Semi-structured interviews will also be conducted with CEA operations across the U.S. to gather information about current practices and potential food safety gaps. Academic researchers and regulatory experts in food safety will also be consulted. The result will be a final synthesis of the available knowledge to provide key takeaways, evidence-based practices, and knowledge gaps on microbial risks during indoor leafy green production.

Food crop production in controlled environments is an increasingly important sector of U.S. and global agriculture. According to the 2019 Census of Horticultural Specialties, sales from “food crops grown under protection” were roughly $700 million in the U.S. These crops include primarily tomatoes, lettuce, cucumbers, peppers, berries, and herbs and account for 54% of the total production (cwt) in the U.S. Controlled environment agriculture (CEA) takes advantage of technologies and automation to modify production climates, shield crops from biotic and abiotic stresses, and optimize environmental factors that maximize plant yield and quality. Greenhouses and indoor warehouses or shipping containers are common CEA structures, and hydroponics, soilless substrate culture, and vertical farming systems are common CEA growing systems. Although CEA helps exclude pests and diseases from produce, pathogen issues can still occur in these operations. Foodborne pathogens enter CEA similar to field-grown crops via: (i) contaminated water, (ii) unsanitary equipment, (iii) contaminated incoming materials such as seeds or plant materials, (iv) employees and staff, and (v) insects and animals. To address this need, we will identify both best practices and research gaps in the peer-reviewed literature, technical abstracts, and grey literature. Semi-structured interviews will also be conducted with CEA operators producing leafy greens across the U.S. to gather information about current practices and potential food safety gaps. Academic researchers and regulatory experts in food safety will also be consulted. The result will be a final synthesis of the available knowledge to provide key takeaways, evidence-based practices, and knowledge gaps on microbial risks during indoor leafy green production.

1. Identify peer-reviewed literature, technical abstracts, and grey literature relevant to foodborne pathogen prevention and control in controlled environment agriculture (CEA). 

2. Conduct semi-structured interviews with CEA leafy greens–producing operations to identify common themes related to microbial risks. 

3. Collaborate with academic researchers and regulatory experts in food safety to further rank the most critical CEA research needs. 

4. Synthesize the available knowledge to provide key takeaways, evidence-based practices, and knowledge gaps on microbial risks during indoor leafy green production.

Finding 1: Investigations on the food safety risks in soilless production systems have typically focused on the potential for pathogens to internalize within edible portion of the leafy greens. Based on the literature review, there is no clear answer regarding the risk of internalization. 

Recommendation 1: We recommend a concerted research effort to tease apart the proposed risk factors for pathogen internalization in leafy greens, including cultivar/variety selection, pathogen type (e.g., selection of serotypes relevant to indoor, soilless production), growth media selection, root colonization, root zone health (i.e., protect from damage), and role of microbial community. 

Finding 2: Published research has focused predominately on risks related to STEC and Salmonella serovars, with relatively fewer (50% less) peer-reviewed articles addressing the risks of L. monocytogenes within indoor, soilless leafy green production. Meanwhile, L. monocytogenes is the primary pathogen responsible for CEA-grown leafy green product recalls. 

Recommendation 2: We recommend that additional research be conducted to characterize the transfer, colonization, and persistence of L. monocytogenes within indoor production systems, along with the critical routes responsible for the introduction of L. monocytogenes into these environments. 

Finding 3: There is little information regarding microbial risks associated with material selection and reuse within indoor, soilless leafy green production. For instance, DWC systems often utilize Styrofoam rafts that are reused until deemed unsuitable via visual inspection versus NFT systems that utilize gutters composed of vinyl (food-grade PVC, but there are DIY options that suggest retro-fitting gutters from home improvement stores). However, there is no guidance on material selection and reuse. 

Recommendation 3: We recommend a characterization of common surfaces within indoor, soilless production systems to evaluate cleanability, appropriate sanitizer chemistries, environmental monitoring strategies, and indicators/signs indicating a given material should be replaced. 

Finding 4: The use of hydrogen peroxide is a common application for both sanitization and plant health by producers, with no standards along with limited support of scientific data. 

Recommendation 4: Immediate studies should be conducted to assess the use of hydrogen peroxide within the CEA environment, with a focus on control of human pathogens. Limits and safe application procedures should be a top priority. 

Finding 5: Risk of contamination is dependent on CEA system type (e.g., DWC, shallow water culture, NFT, vertical, etc.) in addition to management practices. 

Recommendation 5: Risk-based approach to system selection and management should be the goal of the CEA industry. 

Finding 6: The training and educational needs of the CEA industry are not currently being met. Although, recently, new training and outreach materials have become available, these materials are either not reaching the end users or are perceived as too generic or not applicable to the workforce. 

Recommendation 6: More CEA-specific training and outreach materials should be developed with the help of academia, producers, and regulatory experts and shared as open access. In addition, materials should be optimized for the target workforce employed by CEA operations with socially driven missions (e.g., many employ disabled and neurodiverse persons). 

Finding 7: CEA producers are not aware of the Cooperative Extension Service and the types of activities provided by universities to improve CEA food safety. 

Recommendation 7: Extension and outreach programs of universities should be increased for CEA leafy green production, and producers should be contacted to inform about these programs.