Survival and Persistence of Foodborne Pathogens in Manure-Amended Soils and Prevalence on Fresh Produce in Certified Organic Farms: A Multi-Regional Baseline Analysis

Abstract

Biological soil amendments of animal origin (BSAAOs), including untreated (e.g., raw or aged manure, or incompletely composted manure) and treated animal products (e.g., compost), are used for crop production and as part of soil health management. Application of BSAAO's must be done cautiously, as raw manure commonly contains enteric foodborne pathogens that can potentially contaminate edible produce that may be consumed without cooking. USDA National Organic Program (NOP) certified production systems follow the 90-or 120-day interval standards between applications of untreated BSAAOs and crop harvest, depending on whether the edible portions of the crops are in indirect or direct contact with the soil, respectively. This study was conducted to evaluate the survival of four foodborne pathogens in soils amended with BSAAOs and to examine the potential for bacterial transfer to fresh produce harvested from USDA NOP certified organic farms (19) from four states. Only 0.4% (2/527) of produce samples were positive for L. monocytogenes. Among the untreated manure and compost samples, 18.0% (42/233) were positive for at least one of the tested and culturable bacterial foodborne pathogens. The prevalence of non-O157 STEC and Salmonella in untreated manure was substantially > that of E. coli O157:H7 and L. monocytogenes. Of the 2,461 soil samples analyzed in this study, 12.9% (318) were positive for at least one pathogen. In soil amended with untreated manure, the prevalence of non-O157 STEC [7.7% (190) and L. monocytogenes (5.0% (122), was > that of Salmonella (1.1% (26)] or E. coli O157 [0.04% (1)]. Foodborne pathogen prevalence in the soil peaked after manure application and decreased significantly 30 days post-application (dpa). However, non-O157 STEC and L. monocytogenes were recovered from soil samples after 90 and 120 dpa. Results indicate that produce contamination by tested foodborne pathogens was infrequent, but these data should not be generalized outside of the specific wait-time regulations for organic crop production and the farms studied. Moreover, other sources of contamination, e.g., irrigation, wildlife, environmental conditions, cropping and management practices, should be considered. This study also provides multi-regional baseline data relating to current NOP application intervals and development of potential risk mitigation strategies to reduce pathogen persistence in soils amended with BSAAOs. These findings contribute to filling critical data gaps concerning occurrence of fecal pathogens in NOP-certified farming systems used for production of fresh produce in different US regions.

Whole genome characterization of thermophilic Campylobacter species isolated from dairy manure in small specialty crop farms of Northeast Ohio

“…The majority of the Campylobacter isolates (57.3%) from this study possessed multiple drug resistance genes (especially, blaOXA-61 , tetO , and aadE ) based on conventional PCR analysis. Thus, our previous study, as well as studies conducted by other groups, have highlighted the potential public health and food safety risks associated with the use of biological amendments in SSCF ( Ramos et al, 2019 , 2021 ; Black et al, 2021 ; Hailu et al, 2021 ).…”

Risk factors associated with the prevalence of Shiga-toxin-producing Escherichia coli in manured soils on certified organic farms in four regions of the USA

“…A 21-month longitudinal, multi-regional field study was conducted on 19 USDA-NOP certified farms located in four USA regions (California, Minnesota, Maine, and Maryland) during two growing seasons (March 2017-December 2018. Details on the recruitment, study design and farm enrollment can be found in a previous publication (Ramos et al, 2021). Briefly, farms were enrolled based on the following criteria: (1) certified USDA-NOP fresh produce farm, (2) use of untreated manure (i.e., raw or untreated manure), (3) grow at least one of the following fresh crops: leafy greens, root vegetables, and/or fruits, (4) willingness to participate and provide biological samples (raw manure, soil, irrigation water, and fresh produce) and information about their farm management practices and location.…”

Safety Level of Microorganism-Bearing Products Applied in Soil-Plant Systems

“…The main reason is the difference between the recommended treatment procedures by the authorities and their practical use. For example, in a recent analysis, Ramos et al (2021) reported that farmers frequently consider the manure aging (storage time needed to reduce the manure pathogenicity) as composting thus introducing live microorganisms existing in the “treated” material into the soil. Moreover, particularly in Spain, illegal or sub-standard landfilling is still widespread practice with all risks of water, air, and soil contamination and potential health problems for animals and humans ( EC Country Report Spain, 2019 ).…”

“…For these reasons, and particularly in case of factory farming, it is recommended to clean manure, normally by biological or thermal treatment ( Venglovsky et al, 2006 ). In any case, management of manure during storage and further treatment (e.g., by composting) and its proximity to plants from one side, and the always existing possibility of runoff, formation of contaminated dust, and animal movements from the manure storage to crop fields, on the other side, should be an important consideration when analyzing all safety risks on farm sites ( Ramos et al, 2021 ).…”