Factors That Impact L. monocytogenes in BSAAO: Comparison
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Biological soil amendments of animal origin (BSAAO), such as animal waste or animal-waste-based composts, may contain foodborne pathogens such as Listeria monocytogenes. Due to the ubiquitous nature of Listeria, it is essential to understand the behavior of L. monocytogenes in BSAAO in order to develop preharvest prevention strategies to reduce pathogen contamination. As biological control agents, competitive exclusion (CE) microorganisms have been widely utilized in agriculture to control plant- or foodborne pathogens. Due to the diverse microbial community, animal wastes and composts are the potential sources for isolating CE strains for pathogen control. To explore the potential of using CE to control L. monocytogenes in BSAAO.

  • BSAAO
  • compost microbiome
  • competitive exclusion

1. Introduction

Listeria monocytogenes is a significant foodborne pathogen that poses a serious threat to human health. This bacterium is responsible for listeriosis, which can result in a high fatality rate of up to 30% among high-risk individuals [1]. It is commonly associated with and can survive in various foods or food-associated systems, particularly fresh produce [2,3,4,5][2][3][4][5]. Due to the vulnerability of fresh produce to physical decontamination, physical approaches such as pasteurization are typically not applied in preventing pathogen contamination in fresh produce [6,7][6][7]. Additionally, L. monocytogenes can survive and grow in cold temperatures, increasing the risk of contamination of even properly stored produce [8]. Therefore, postharvest control methods are limited for fresh produce and effective preharvest control measures to prevent L. monocytogenes contamination are critical for ensuring fresh produce safety.
Biological soil amendments of animal origin (BSAAO) including raw animal manures and composts are commonly used to enhance the yield of fresh produce and other agricultural crops [9]. However, inadequately treated BSAAO can also be a potential source of L. monocytogenes contamination in fresh produce [10]. While studies have been focused on the fate of L. monocytogenes in BSAAO, the essential factors that can impact the persistence of L. monocytogenes in BSAAO have not been comprehensively reviewed [11]. Therefore, it is important to understand the behavior of L. monocytogenes in BSAAO and the potential preharvest prevention measures which can be used for fresh produce.
Raw animal manure contains feces, urine, bedding materials, and other secretions from the animal. As the rich sources of plant nutrients, animal wastes are commonly used as fertilizers or biological soil amendments [12,13][12][13]. However, the application of untreated animal wastes may introduce potential microbial hazards to crop fields; thereby, it is required that the raw animal manure be incorporated into the soil more than 90 days prior to harvest for crops that have no direct contact with soil, and 120 days if the produce has direct contact with soil [14]. The application of raw manure must not contact produce during application, and the potential for contact with produce after application should be minimized [14]. Sheng et al. [15] conducted a 2-year field study to evaluate the impacts of dairy manure fertilizer application on the microbial safety of red raspberries. Although no Shiga-toxin-producing E. coli (STEC) or L. monocytogenes was detected in fertilizer, soil, foliar, or raspberry fruit samples throughout the sampling period of 2 years, Salmonella in soil amended with contaminated fertilizer was reduced to an undetectable level after 2 or 4 months of application.
The harmful or pathogenic microorganisms in BSAAO can be reduced or eliminated through composting. Composting is a controlled biological process that broadly consists of four typical phases based on the temperature generated and active microbial community: mesophilic, thermophilic, cooling, and maturation phases. Normally, composting process proceeds with solid or liquid materials within a moisture level range of 40 to 50% or 90 to 98%, respectively [16]. During a satisfactory composting process, mesophilic, thermophilic, and thermotolerant bacteria, fungi, and actinomycetes are actively involved [17]. Pathogens are killed primarily by the accumulation of heat (45 to 75 °C) generated by indigenous microorganisms during the early phases of aerobic composting of animal manures [18,19,20][18][19][20]. However, due to the complex composting process or the recontamination during storage, the pathogenic bacteria can be reintroduced to the finished compost. As specified by the Food Safety Modernization Act (FSMA) Produce Safety Rule, microbial standards for biological soil amendments of animal origin include less than 0.3 most probable number (MPN) per gram or milliliter of analytical portion for E. coli O157:H7, less than 3 MPN per 4 g or mL of total solids for Salmonella spp., and less than 1 CFU per 5 g or mL of analytical portion for L. monocytogenes [14]. To achieve these standards, the FSMA’s Produce Safety Rule mandates the incorporation of alternative treatments for reducing or eliminating human pathogens in raw animal wastes before land application [21].
Physical and chemical methods for controlling pathogens in BSAAO often have adverse environmental impacts, such as greenhouse gas emissions and odor pollution, and may be costly [11,22][11][22]. To address these challenges, researchers have explored biological methods for reducing or inhibiting pathogen populations in BSAAO [22]. One promising approach is the use of competitive exclusion (CE) microorganisms, in which multiple beneficial microorganisms are allowed to grow and establish a community that can inhibit the growth of pathogens like L. monocytogenes [23,24][23][24]. CE offers a cost-effective and environmentally sustainable means of reducing pathogen populations in BSAAO by leveraging the natural properties of microbiological communities [25]. Moreover, the metabolic activities of microbiological communities in BSAAO can provide essential nutrients for plant growth, making this approach both effective and sustainable [11]. Lactic acid bacteria have been well studied to competitively exclude pathogens like Escherichia coli O157:H7, Salmonella, and L. monocytogenes in foods [26[26][27],27], but their effectiveness against L. monocytogenes in BSAAO is not conclusive. Furthermore, microbial communities, including other species that effectively control L. monocytogenes are unclear.

2. Factors That Impact the Fate of L. monocytogenes in BSAAO

The presence of L. monocytogenes has been reported in both pre- and post-harvest environments, including fresh vegetables, processing environments, soil, animal feces, and irrigation water [3,28,29][3][28][29]. Studies from the last 20 years have reported that animal wastes or associated produce fields can become contaminated with L. monocytogenes, and the prevalence level ranged from 0 to 50% [3,29,30,31,32,33,34,35,36,37][3][29][30][31][32][33][34][35][36][37]. Livestock manure and manure-contaminated water have been identified as potential sources of high levels of L. monocytogenes [36]. L. monocytogenes was often isolated from both farm and processing environments because it can mediate a saprophyte-to-cytosolic-parasite transition by modulating the activity of a virulence regulatory protein called PrfA, using available carbon sources [38,39,40][38][39][40]. L. monocytogenes can form biofilms, allowing it to establish and persist for extended periods in various environments [41]. A comprehensive understanding of the survival characteristics of L. monocytogenes is therefore crucial reducing food contamination with this pathogen. The growth and survival of L. monocytogenes on fresh produce have been extensively reviewed [40,42][40][42]. Worldwide, the prevalence of L. monocytogenes in fresh produce was 0.9 to 25%, and the highest level was identified in parsley in Malaysia [40,43][40][43]. The growth and survival of L. monocytogenes on intact fresh produce varied depending on the type of commodity, and the highest growth rates were observed at temperatures of 20 °C or higher. Importantly, both of these studies suggested that L. monocytogenes contamination on fresh produce can occur directly or indirectly via fecal and compost contamination. Therefore, it is essential to identify the factors that can significantly affect the survival of L. monocytogenes in animal wastes and composts derived from animal waste to better understand the fate of this pathogen in such materials. According to the challenge studies published from 2000 to 2023 on the fate of L. monocytogenes in BSAAO, the initial level of spiked pathogens ranged from 2 to 8 log CFU/g or mL, depending on the research purpose (Table 1). The factors that influenced the fates of L. monocytogenes in BSAAO can be grouped as follows: (i) Types and physical-chemical characteristics of BSAAO; (ii) storage temperature of BSAAO; and (iii) background microbial community in BSAAO. Depending on these factors and experimental design, pathogens in animal wastes or composts derived from animal waste can survive better in dairy manure, at a lower temperature, and with a reduced background microbial load. Notably, most of the studies were carried out for the evaluation of several confounding factors together. Microbial growth and metabolic processes depend on moisture content and nutrients. Factors including moisture content (ranging from 20 to 80%), water activity (ranging from 0.89 to 0.75), and extra organic matter (ranging from 2 to 7%) [44,45,46,47,48,49,50][44][45][46][47][48][49][50] have shown the impacts on the survival of L. monocytogenes in different types of animal waste. Dairy slurries can support L. monocytogenes survival for up to 28 days at 25 °C, compared to other animal wastes like those from pigs, poultry, or sheep [44,47][44][47]. L. monocytogenes were unchanged in the sawdust manure mix and untreated liquid swine manure for up to 28 days at 25 °C [44]. Adding 2% dry matter (e.g., hay, straw, or bedding materials) enhanced pathogen survival [50]. Most importantly, it is not surprising that the microbiota in BSAAO can also be impacted by the aforementioned factors and therefore impact the pathogen survival. BSAAO, in the form of animal manure or animal-waste-based compost, can be considered a rich source for microbiomes. Microbial species, such as Aeromonas hydrophila, Arobacter butzleria, Bacillus anthracis, Brucella abortus, Campylobacter jejuni, Chlamydia psittaci, Clostridium perfringens, Clostridium botulinium, Coxiella burneti, E. coli, and Yersinia spp., were found in animal manure or animal waste [12]. During the composting process, mesophilic bacteria (i.e., Pseudomonaceae, Erythrobacteraceae, Comamonadaceae, Enterobacteriaceae, Streptomycetaceae, and Caulobacteraceae families) could break down the organic matter in the initial stage [51]. In the finished compost, the typical microorganisms presented include Alcaligenes faecalis, Arthrobacter, Brevibacillus, Enterobactericae, Bacillus species, Thermus spp., Streptomyces, Aspergillus fumigatus, and Basidiomyces spp., which belong to groups of bacteria, actinomycetes, or fungi [52]. The type of raw manure can significantly impact the microbial members in the finished compost product; for example, Proteobacteria and Chloroflexi were the major phyla in sheep and cattle manure composts, and Firmicutes dominated in pig and chicken manure composts [53]. Some of these active microbial members in BSAAO, such as Bacillus or actinomycetes, can surely impact the behaviors of invasion pathogens present in the BSAAO by competition or other mechanisms. Many studies have shown that the fate of L. monocytogenes in animal manure and the BSAAO-amended soil ecosystem was affected by the composition of background microbial communities [54,55,56,57,58][54][55][56][57][58]. In most cases, the reduced indigenous microbial load favored the persistence of pathogens in animal manure or BSAAO-amended soil. For example, the quick die-off of pathogens in nonsterile soil was mostly due to the antagonistic effects against L. monocytogenes by the indigenous microflora. In contrast, Desneux et al. [54] found that the behavior of L. monocytogenes was not influenced by the taxonomic composition of pig manure. The authors suspected that L. monocytogenes entered a viable but non-culturable stage in the pig manure during storage. However, modifications in the indigenous microbial community, such as autoclaving or diluting, omitted effects on the natural microbiota. As such, the complex interactions between the invasion pathogens and indigenous microflora still require further research. Because amending agriculture soil with treated animal manure instead of fresh manure released less potential Listeria in the environment [59], biological treatment options, including composting (aerobic) and biogas (anaerobic) processes, can be used as pathogen control treatments in addition to recycling raw animal wastes back into the soil for crop use. The finished compost should be thoroughly decomposed and thereby pathogen-free. However, sporadic cases have been reported of the presence of foodborne pathogens in finished compost, indicating that the inadequately treated composts made from animal waste are potential sources for pathogens [58,59][58][59]. These pathogens either survived the composting process or were cross-contaminated with raw manure, and had growth potential during the storage of the compost. To meet the microbial standards for BSAAO, the incorporation of alternative treatments, such as competitive exclusion strategies, for reducing or eliminating human pathogens in raw animal wastes before land application is required [21].
Table 1. Summary of reported studies on the factors affecting survival of L. monocytogenes in animal wastes and animal-wastes-based compost (2000 to 2023) 1.
Matrix Used Initial Levels Treatment Significant Findings Reference
Bovine-manure-amended soil 5 to 6 log CFU/g Temp: 5, 15 or 21 °C;

BMC: manure-amended autoclaved soil		 L. monocytogenes survived longer at lower temperatures in the manure-amended autoclaved soil. [55]
Pig manure N.A. Temp: 8 and 20 °C;

AWT: raw and biological treated manures;

BMC: 81.5–94.8% and 67.8–79.2% VBNC cells		 L. monocytogenes increased more at 20 °C.

L. monocytogenes can enter VBNC state in the pig manure during storage and the behavior of L. monocytogenes was not influenced by the taxonomic composition of pig manure.		 [54]
Dairy manure compost 7.4 log CFU/g ST: Solid or liquid manure with different compost pile size L. monocytogenes can survive in solid manure pile for at least 29 weeks; compost pile size and temperature affect the pathogen survival. [60]
Composted livestock manure or sewage sludge 5–6 log CFU/g Temp: 50 °C;

TD: 3 months;

AWT: dairy cattle, beef cattle, pig, poultry layer, and sheep		 Pathogen survival time order (shorter to longer): dairy cattle = pig < poultry layer = sheep < beef cattle. [49,61][49][61]
Farmyard manure (FYD) 2.1–4.9 log CFU/mL AWT: dairy FYD, pig FYD, broiler liter, dairy slurry, and dirty water Maximum pathogens survival period during storage: dairy FYD = pig FYD (regardless turned or unturned) < broiler litter < dairy slurry with 7% dry matter < dairy slurry with 2% dry matter. [50]
Liquid swine manure and sawdust manure mix and dairy manure compost 6 log CFU/g ST: sawdust manure mix or untreated swine manure or pack storage;

Temp: 25 to 55 °C		 L. monocytogenes were unchanged in the sawdust manure mix and untreated liquid swine manure for up to 28 days at 25 °C.

L. monocytogenes was destroyed most rapidly under thermophilic composting and persisted the longest in pack storage or low-temperature composting.		 [44,47][44][47]
Dairy compost extract 3 log CFU/mL Temp: 22 to 35 °C;

AWT: water extract of dairy compost of different ratios (1:2,1:5, and 1:10, w/v)		 Indigenous microflora suppressed the pathogen regrowth in compost extract, especially at 35 °C. [62]
Animal-manure-based compost 7 log CFU/g Temp: 20 to 40 °C;

MC: 30 to 60%;

AWT: dairy, chicken, and swine compost mixed with supplements		 Volatile acids promoted pathogen inactivation when temperatures were too low or quick heat was lost at the surface of compost piles.

Suboptimal MC (30–40%) were less effective for pathogen inactivation.		 [63,64][63][64]
Dairy manure 7 log CFU/mL Temp: 30, 35, 42, and 50 °C;

ST: anaerobic (AN) and limited aerobic (LA)		 Temp: Reduction in PA increased with higher temperature.

ST: Effects of both LA and AN condition in pathogen reductions were similar.

Pathogen survival time order (shorter to longer) was: L. monocytogenes < Salmonella < E. coli.		 [48]
Anaerobic Biogas Digestates 7 log CFU/g Temp: 1.1 to 19.1 °C

AWC: pig, cattle, poultry, and horse slurry mixed with maize silage		 Temp: Reduction in PA increased with higher temperature.

Pathogen survival time order (shorter to longer) was: Salmonella < E. coli < L. monocytogenes.		 [65]
1 Temp, Temperature; MC, Moisture content level; ST, Storage condition; BMC, Background microbial community; SE, Season; TD, Testing duration; AWT, Animal waste types.

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