ABSTRACT

Listeria monocytogenes may be present in produce-associated environments (e.g., fields, packing houses); thus, understanding its growth and survival on intact, whole produce is of critical importance. The goal of this study was to identify and characterize published data on the growth and/or survival of L. monocytogenes on intact fruit and vegetable surfaces. Relevant studies were identified by searching seven electronic databases: AGRICOLA, CAB Abstracts, Center for Produce Safety funded research project final reports, FST Abstracts, Google Scholar, PubMed, and Web of Science. Searches were conducted using the following terms: Listeria monocytogenes, produce, growth, and survival. Search terms were also modified and “exploded” to find all related subheadings. Included studies had to be prospective, describe methodology (e.g., inoculation method), outline experimental parameters, and provide quantitative growth and/or survival data. Studies were not included if methods were unclear or inappropriate, or if produce was cut, processed, or otherwise treated. Of 3,459 identified citations, 88 were reviewed in full and 29 studies met the inclusion criteria. Included studies represented 21 commodities, with the majority of studies focusing on melons, leafy greens, berries, or sprouts. Synthesis of the reviewed studies suggests L. monocytogenes growth and survival on intact produce surfaces differ substantially by commodity. Parameters such as temperature and produce surface characteristics had a considerable effect on L. monocytogenes growth and survival dynamics. This review provides an inventory of the current data on L. monocytogenes growth and/or survival on intact produce surfaces. Identification of which intact produce commodities support L. monocytogenes growth and/or survival at various conditions observed along the supply chain will assist the industry in managing L. monocytogenes contamination risk.

HIGHLIGHTS
  • L. monocytogenes growth and/or survival on intact produce differed by commodity.

  • Intact produce held at ≥20°C had the highest L. monocytogenes growth rates.

  • Produce surface and storage conditions affected L. monocytogenes growth and/or survival.

  • Microbial carrying capacity is crucial to characterizing growth and/or survival patterns.

  • Studies need to describe experimental conditions (e.g., relative humidity) for modeling efforts.

Listeriosis is the leading cause of reported bacterial foodborne disease–related deaths each year in the United States (88). There are an estimated 1,600 cases of listeriosis in the United States annually, with a mortality rate of approximately 20% (88). Less than 1% of recorded foodborne outbreaks in the United States was linked to produce during the 1970s (32), but from 1990 to 2005, fruit and vegetable products were responsible for an estimated 13% of foodborne outbreaks (32). Increased consumption and availability of fresh fruits and vegetables may have contributed to this increase: between 1970 and 2016, the U.S. Department of Agriculture (USDA), Economic Research Service estimated increases in per capita availability of fresh fruits and vegetables at approximately 40 and 20%, respectively (110). Listeria monocytogenes also constitutes a considerable economic burden to society. The economic burden of foodborne illness in the United States is estimated at approximately $78 billion, with the economic burden specific to listeriosis predicted at >$2.8 million annually (109).

L. monocytogenes has been isolated from a variety of environments, including produce production (97), urban (87), natural (27), processing (62), and retail (92), so there are numerous opportunities for food to become contaminated throughout the supply chain. Control of growth and/or survival of L. monocytogenes is essential in minimizing large-scale contamination events. This is especially true for ready-to-eat (RTE) foods such as produce that are often consumed raw or with minimal processing. Produce-borne L. monocytogenes outbreaks were historically associated with processed produce products, such as coleslaw (89) or diced celery (43), but in the last decade, L. monocytogenes has been associated with contaminated whole, intact produce including cantaloupe, stone fruit, and caramel apples (20, 21, 56). A 2011 outbreak of listeriosis, affecting 28 states, was due to consumption of cantaloupe produced by Jensen Farms in Colorado (20). The cantaloupe-borne outbreak caused 147 illnesses and 33 deaths, making it the deadliest outbreak of foodborne illness to occur in the United States in the past 25 years (20). A 2014 recall of stone fruit (whole peach, nectarine, plum, and pluot) occurred due to potential L. monocytogenes contamination. Pulsed-field gel electrophoresis (PFGE) types from the recalled stone fruit had exact PFGE matches to four listeriosis patients in PulseNet USA, and two of these cases were linked to the recalled stone fruit (15, 56). Table 1 provides a historical summary of U.S. and worldwide L. monocytogenes outbreaks associated with the consumption of contaminated whole and fresh-cut produce. It is clear from Table 1 that a majority of fresh produce–linked L. monocytogenes outbreaks are associated with produce that is cut, processed, or sprouted. There are only four outbreaks associated with intact produce, and these were linked to melons (3) or stone fruit (1).

TABLE 1

Outbreaks of listeriosis associated with produce consumption

Outbreaks of listeriosis associated with produce consumption
Outbreaks of listeriosis associated with produce consumption

It is well understood that fruits and vegetables are grown in environments where L. monocytogenes may be present, albeit sporadically and in low numbers (37). Although the produce production environment is generally not ideal for growth of pathogens, specific environmental factors and management practices can promote growth and/or survival conditions (12, 27, 7577). However, it is unrealistic to assume that intact fruits and vegetables will not become contaminated; therefore, it is important to consider how intact produce postharvest handling practices and storage conditions may amplify risk from these infrequent, sporadic, low-level contamination events. Pathogen growth may be impacted by temperature, competitive microflora, humidity, water activity, and pH, among other factors (53); thus, the produce industry seeks to understand L. monocytogenes growth and no-growth conditions as well as parameters that enhance L. monocytogenes survival on intact, whole fruits and vegetables. Identification of conditions favorable to the growth and survival of L. monocytogenes will allow for development of best practice mitigations and highlight future research needs. Furthermore, information on L. monocytogenes behavior on whole, intact fruits and vegetables will assist regulatory agencies and industry groups in risk assessment and management decisions.

The objective of this study was to perform a systematic literature review to identify and characterize published data on the growth and/or survival of L. monocytogenes on whole, intact fruit and vegetable surfaces. Whereas other reviews (15, 53, 72, 77) have described L. monocytogenes risk factors in RTE foods (e.g., fresh-cut produce) and environmental factors contributing to the contamination of produce, our review focuses on intact, whole fruits and vegetables and characterizes the risk factors that promote pathogen growth and/or enhanced survival on their surfaces. In addition, the study herein aims to identify future research needs including areas where data are lacking for various produce commodities or where data are missing for typical commodity handling and storage parameters observed along the produce supply chain.

MATERIALS AND METHODS

Literature search

This systematic literature review was conducted according to the guidelines of the Centre for Reviews and Dissemination (26). Publications were identified by searching seven databases: Ovid CAB Abstracts (beginning 1910), Center for Produce Safety funded research project final reports (beginning 2008), EBSCO AGRICOLA (beginning 1978), Ovid Food Science and Technology Abstracts (beginning 1969), Google Scholar, PubMed (beginning 1949), and Web of Science (beginning 1990) through January 2019 (15, 53, 77). Searches were conducted using three Medical Subject Heading terms: Listeria monocytogenes, growth, and survival. These were combined with intact, whole fresh produce–associated Medical Subject Heading terms (fruit, vegetable, raw agricultural commodity, produce, preharvest, fresh, whole, intact). All Medical Subject Heading search terms were modified for each database thesaurus and were “exploded” to find all related subheadings (e.g., Listeria in addition to L. monocytogenes). We reviewed the references of published reviews, reports, and original and short communication research articles to identify additional studies. Studies not published in English were translated by either Virginia Tech appropriate staff and/or Google Translator (Google Inc., Mountain View, CA; https://translate.google.com).

Study selection

Studies had to be relevant to the growth and/or survival of L. monocytogenes on whole, intact fruit and vegetable surfaces. Studies had to include sufficient and reproducible information on methodology (e.g., inoculation methods) and experimental conditions (e.g., storage temperatures) and demonstrate quantitative growth and survival data (e.g., log CFU per gram) over time to be eligible for selection. Pertinent data from studies where the control group fit or partially fit the selection criteria were included for review. Conference abstracts, reports (e.g., Center for Produce Safety final grant reports), theses, and dissertations were also reviewed for selection if data were not duplicated in research manuscripts. Studies were not selected for inclusion if methods were unclear or inappropriate (e.g., dip inoculation studies were excluded because they may facilitate infiltration, especially at the stomata and stem scar). Spot and spray inoculations tend to minimize distribution of microbial cells at these sites and enable a more accurate determination of the reduction in pathogen population (35, 60, 61). All candidate studies that were selected were reviewed, and duplicates, patents, and books and book chapters were excluded by one author (C.M.M.). Titles and full abstracts of remaining candidate studies were then independently examined in detail for final inclusion by two authors (C.M.M. and J.Z.). Another author (L.K.S.) merged the included study lists by C.M.M. and J.Z. Any disagreements between the two reviewers were handled by group discussion led by L.K.S. until consensus (C.M.M., J.Z., and L.K.S.) was achieved. The full text of each candidate study granted full inclusion was reviewed again before final inclusion.

Extraction and synthesis of data

All data were extracted from the texts (e.g., manuscripts, reports) for studies achieving final inclusion. Studies were evaluated individually and not pooled. Data were extracted on produce type, inoculation matrix and procedure, enumeration methodology, storage temperature, storage relative humidity (RH), sample collection time points (e.g., 1, 2, and 3 days), L. monocytogenes population counts (log CFU per produce piece or gram), total and/or rate of L. monocytogenes population change, location of study (e.g., state, country), and any other relevant experimental condition(s). Data were entered into Excel (Microsoft Corp., Redmond, WA). Authors (L.K.S and D.W.S.) performed a quality assessment on extracted data with guidelines from the Centre for Reviews and Dissemination (26) and Sargeant et al. (85, 86). When studies did not provide tabular data for L. monocytogenes growth and/or survival on intact, whole fruit and vegetable surfaces, data from figures were extracted using Web Plot Digitizer (Ankit Rohatgi, San Francisco, CA; https://apps.automeris.io/wpd/). Data from individual studies were analyzed using JMP Pro 14 statistical software (SAS Institute Inc., Cary, NC). An analysis of variance and Tukey's multiple comparison test were performed. Growth and/or survival rates were obtained using DMFit (7). Because most studies were conducted with diverse measurements, statistical pooling of the outcomes was not performed. The risk factors contributing to L. monocytogenes growth on whole was discerned based on the conclusions of individual studies.

RESULTS

Selection of eligible studies

In total, 3,459 documents were identified in the first, primary search (Fig. 1). After the removal of duplicates including articles, abstracts, and reports (n = 1,581), books and book chapters (n = 262), and patents (n = 14), 1,602 relevant documents remained. All 1,602 remaining titles and abstracts were examined and were removed if selection criteria were not met. In total, 88 potentially relevant articles were reviewed in full by two independent reviewers who reached consensus. Documents were excluded or removed for various reasons (Fig. 1), including irrelevant microorganisms, treatment, and use of fresh-cut produce, among other reasons. Fifty-nine documents were excluded including (i) use of cut produce or juice (n = 24), (ii) unclear or inappropriate methods (n = 21), (iii) insufficient data (n = 9), (iv) duplicate data (n = 3), and (v) incorrect document (e.g., comment, editorial, protocol; n = 2). Documents were removed if data were duplicated in both a report and manuscript and/or judged unreproducible due to insufficient methodology. Twenty-nine documents were determined adequate for inclusion in this review.

FIGURE 1

Schematic representation showing selection of studies through the process of the systematic literature review.

FIGURE 1

Schematic representation showing selection of studies through the process of the systematic literature review.

Characteristics of included studies

Details of the 29 selected documents are summarized in Table 2, including data on temperature, relative humidity, study duration, sample collection time points, storage, and reported L. monocytogenes population outcome(s). Studies included 21 unique fruit and vegetable commodities: apples var. Gala and Granny Smith (1); asparagus (1); Haas avocado (1); blueberries (1); canary melons (1); cantaloupe melons (4); celery (1); cranberries (1); cucumbers (2); jalapenos (1); kale (1); lettuce (1); mangoes var. Ataulfo, Kent, and ‘Tommy Atkins' (2); mushrooms (Agaricus bisporus) (1); nectarine var. August Fire (1); peach var. Autumn Flame (1); persimmons (1); raspberries (1); spinach (3); sprouts (4); and strawberries (1).

TABLE 2

Summary of studies on growth and survival of L. monocytogenes on produce surfaces

Summary of studies on growth and survival of L. monocytogenes on produce surfaces
Summary of studies on growth and survival of L. monocytogenes on produce surfaces

Factors associated with growth and survival: surface structure

Several studies (5, 38, 39, 45, 65, 66, 68, 71, 73, 74, 82, 114) examined the growth and/or survival of L. monocytogenes as it relates to surfaces structure. Data were available on the influence of surface structure on L. monocytogenes growth for avocado, cantaloupe, cucumber, lettuce, mango, mushrooms, strawberry, spinach, and sprouts (5, 38, 39, 45, 65, 66, 68, 71, 73, 74, 82, 114).

The topographic characteristics of cantaloupes may have had an effect on the observed population dynamics. Martinez et al. (68) speculated that the rind surface of the cantaloupe, with its extensive netting, may have promoted attachment, biofilm formation, and growth of L. monocytogenes. Nyarko et al. (71) similarly attributed the rough ridges on the rind surfaces of cantaloupes to facilitate microbial attachment. These authors hypothesized that the L. monocytogenes may have been less affected by desiccation stress related to storage temperature and thus exhibited slower population decline (71). Hydrophobicity also strongly influences the movement and distribution of microorganisms. Both the waxy cuticular surface of mangoes and the thick, shell-like, waxy skin of avocadoes are hydrophobic; the outer surface of these two commodities functions as a permeable barrier against moisture and gas loss and provides the ability to repel water (45, 82).

The nutrient availability on the surface of produce commodities differs and may have an effect on population dynamics. Likotrafiti et al. (65) studied the dynamics of L. monocytogenes on cucumber and lettuce, where L. monocytogenes growth was observed on cucumber epidermis, but not on lettuce. The authors speculated that this was due to differences in nutrient availability on the surface of the different vegetables (65). Differences in surface structure and availability of surface moisture and/or nutrients may also explain the inability of L. monocytogenes to grow on intact strawberries compared with other fruits with high-moisture surfaces (38). Other studies (39, 66, 114) suggest limited nutrient availability on the surface of intact fruit and vegetable outer surfaces (cantaloupes, celery, and sprouts) may have limited the growth of L. monocytogenes.

The growth of L. monocytogenes on produce surfaces may be affected by competition with the natural microbial population. Aytac and Gorris (5) observed that the behavior of L. monocytogenes on sprouts was affected by the initial microflora load, with the L. monocytogenes proliferating better on sprouts with lower background microflora. Francis and O'Beirne (39) also attributed the inability of sprouts to support L. monocytogenes growth to competition from high populations of background microflora (108 CFU/g). Cantaloupes and mushrooms also showed the same trend: a lack of L. monocytogenes growth with high populations of competitive background microflora on the surface (46, 66, 71). Background microflora on the surface of spinach did not inhibit the growth of L. monocytogenes; however, it did decrease the growth rate (73, 74). The maximum growth rate of L. monocytogenes on spinach decreased as the initial concentration of total mesophilic bacteria increased (73, 74).

The attachment of L. monocytogenes (and therefore its ability to grow and survive) on the surface of fresh produce may differ depending on specific produce surface properties. Generally, increasing surface roughness and nutrient availability better supported L. monocytogenes growth and/or survival, whereas increased hydrophobicity (i.e., waxy surfaces) and competitive background microflora limited L. monocytogenes growth and/or survival on the surface of intact, whole fruits and vegetables.

Factors associated with growth and survival: storage temperature

Storage conditions, including temperature and relative humidity, are two of the most important environmental factors needed to maintain the quality and shelf life of produce (4, 65, 78, 102, 120). Table 3 displays the growth rates for produce commodities at three common storage temperatures along the supply chain: 4 ± 2°C (refrigeration), 10 ± 2°C (open case, refrigeration), and ≥20°C (ambient). Growth rates for produce data at temperatures not included within the three ranges were excluded from Table 3.

TABLE 3

Growth rate and standard deviations for all reported produce commoditiesa

Growth rate and standard deviations for all reported produce commoditiesa
Growth rate and standard deviations for all reported produce commoditiesa

Twenty-seven studies (representing 19 commodities) included in this review examined the fate of L. monocytogenes populations at more than one storage temperature (ranging from −20 to 36°C), and two commodities included data at only one storage temperature: avocado (22°C) and cranberry (4°C). Only 3 of the 19 produce commodities demonstrated L. monocytogenes growth at all storage temperatures tested within each individual study: canary melons (5, 15, 20, 30, and 35°C), kale (4 and 7°C), and persimmons (10, 20, and 30°C) (67, 90, 103). Although varying storage temperature had no significant (P > 0.05) effect on L. monocytogenes populations on the surface of kale (67), increasing storage temperature did significantly increase (P ≤ 0.05) the growth of L. monocytogenes on canary melon and persimmon surfaces (90, 103). Because the two temperatures in the kale study (4 and 7°C) are both considered refrigeration and quite similar, the absence of a temperature to L. monocytogenes population correlation is not surprising.

Seven commodities demonstrated L. monocytogenes survival at all experimental storage temperatures tested within each individual study: apples (5 and 25°C), blueberries (4 and 12°C), lettuce (10, 20, and 30°C), mushrooms (4 and 10°C), nectarines (20 and 30°C), peaches (20 and 30°C), and strawberries (4 and 24°C) (1, 29, 38, 46, 65, 83). Interestingly, reductions of L. monocytogenes populations on intact strawberries were significantly faster (P ≤ 0.05) at a higher storage temperature (24°C) compared with at a lower storage temperature (4°C) (38). Unlike for strawberries, storage temperature did not significantly (P > 0.05) affect the survival of L. monocytogenes on the surface of apples, blueberries, lettuce, mushrooms, nectarines, and peaches (1, 29, 46, 65, 83).

Nine commodities demonstrated both L. monocytogenes growth and/or survival, with population dynamics varying with different storage temperatures. Only one study each was performed to investigate L. monocytogenes growth and/or survival on the surface of asparagus (19), celery (114), jalapeno (55), and raspberry (70) versus multiple studies for cantaloupe (68, 71), cucumber (8, 65), mango (30, 82), spinach (73, 74), and sprouts (39, 100, 101). L. monocytogenes population behavior trends for a specific commodity were similar between studies for cucumber, spinach, and sprouts, except mango and cantaloupe. For example, on the surface of mango, Rangel-Vargas et al. (82) reported L. monocytogenes survival, but no growth at 3 and 25°C, whereas Danyluk (30) observed L. monocytogenes growth at 12, 20, 25, and 30°C. Nyarko et al. (71) found the population of L. monocytogenes on cantaloupe rinds were not significantly (P > 0.05) different at 4, 10, and 25°C, whereas Martinez et al. (68) found growth of L. monocytogenes was significantly higher (P ≤ 0.05) on the rind surface at 8 and 25°C over 7 days compared with 21 days at 4°C.

Factors associated with growth and survival: storage relative humidity

Limited information is available regarding the effect of relative humidity on the survival of L. monocytogenes on vegetables. Only one study examined the effect of relative humidity on the growth and/or survival of L. monocytogenes on intact cucumber and lettuce (65). Both cucumber and lettuce data indicated low relative humidity decreased the growth rate and increased the death rate of L. monocytogenes on produce surfaces (65). L. monocytogenes populations remained relatively constant on cucumber epidermis at 53% RH but increased significantly (P ≤ 0.05) at 90% RH after samples were held at 10°C for 3 days (65). Moreover, L. monocytogenes populations on the surface of cucumbers stored at 90% RH were significantly (P ≤ 0.05) higher on day 1 through day 4 than on the surface of cucumbers stored at 53% RH and 20°C (65). Interestingly, L. monocytogenes populations on the surface of lettuce stored at 10°C remained approximately constant at 90% RH, whereas populations declined at 53% RH (65). No significant differences (P > 0.05) in L. monocytogenes populations were observed on the surface of lettuce stored at 53 and 90% RH at 20 and 30°C (65). Results from this study suggest L. monocytogenes populations decrease at low relative humidity, especially at cooler temperatures. Although other studies included in this review reference the relative humidity under which experiments were conducted (Table 2), data were insufficient for assessing relative humidity as a factor associated with L. monocytogenes growth and/or survival on fruit and vegetable surfaces because only one relative humidity condition was used.

Factors associated with growth and survival: storage matrix

The effect of storage container on the growth and/or survival of L. monocytogenes was examined for four produce commodities: asparagus (19), celery (114), mushrooms (46), and sprouts (39). Vandamm et al. (114) investigated the impact of storage containers on the fate of L. monocytogenes on celery under simulated consumer storage conditions. Samples were either sealed within a polyethylene plastic press-to-seal snack bag or a polyethylene “double-seal lidded” container to mimic containers used by consumers (114). No significant difference (P > 0.05) in L. monocytogenes populations was observed between container type regardless of other experimental parameters. Vandamm et al. (114) attributed the findings to the relatively low passive accumulation of CO2 (≤2.4%) within each container type, with no significant difference (P > 0.05) in the atmosphere (O2 and CO2 levels) between the two containers. Francis and O'Beirne (39) examined the atmosphere of packaged sprout samples sealed within oriented polypropylene packaging film. They found that sprouts had a relatively high respiration rate and when sealed in the packaging, air and CO2 levels rose from 0 to 1% to 25 to 27% and O2 levels fell from 20 to 22% to 0 to 1% during the 12-day storage period (39). L. monocytogenes was unable to grow on the packaged sprouts, which may be a result of the high CO2 levels suppressing growth (39). However, Gonzalez-Fandos et al. (46) reported that L. monocytogenes was able to grow between 1 and 2 log units at 4 and 10°C in inoculated mushrooms packaged in perforated and nonperforated polyvinyl chloride films. However, after 10 days of storage, the populations of L. monocytogenes were higher in mushrooms packaged in nonperforated polyvinyl chloride films and stored at 10°C. Although significant differences (P ≤ 0.05) in CO2 and O2 concentrations were found between mushrooms packaged with perforated and nonperforated films, there was a relatively low passive accumulation of CO2 (≤6.5%), similar to the findings of Vandamm et al. (114). Castillejo-Rodriguez et al. (19) determined changes in CO2 and O2 concentrations while monitoring the growth of L. monocytogenes in packaged asparagus. A modified atmosphere was created inside the package during storage, with an increase in the levels of CO2 (from 1.6% to 3.75 to 18.8%) and with a decrease in the O2 concentration (from 18.1% to 17.6 to 6.5%) (19). Growth of L. monocytogenes was not affected by the changed atmosphere (19).

Factors associated with growth and survival: inoculation concentration

The inoculum concentration for all studies examined in this review ranged from 2.1 to 7.6 log CFU/g or produce piece, with an average inoculum concentration of 4.5 ± 1.3 log CFU/g or produce piece. Only three studies (1, 30, 38) investigated the influence of differing inoculum concentrations on L. monocytogenes populations on intact, whole strawberry, peach, nectarine, and mango. Flessa et al. (38) inoculated strawberry samples at two inoculation concentrations, approximately 7.5 log CFU per berry and 5.6 log CFU per berry. At ambient storage temperatures, a significantly faster (P ≤ 0.05) decline in L. monocytogenes populations was observed on strawberry samples inoculated at the lower inoculum concentration (decline of 3.3 log CFU per berry) compared with at the higher inoculum concentration (decline of 1.4 CFU per berry) over 48 h (38). Interestingly, this finding was not duplicated for intact strawberry samples held at the 4°C storage temperature; instead, L. monocytogenes populations declined approximately 3 log CFU per berry for both inocula over 7 days (38). Danyluk (30) observed that L. monocytogenes populations inoculated on mangoes at both high and low inoculum concentrations (∼6 and ∼3 log CFU per mango, respectively) reached similar maximum levels (∼6.5 log CFU per mango) when stored at 25°C. It was hypothesized the observation was the result of reaching the carrying capacity (the maximum population size of bacterium that an environment can sustain, given the recourse available) of L. monocytogenes on mango. Although the prior two studies (30, 38) observed starting inoculum concentration to impact L. monocytogenes growth and/or survival on produce surface, Amalaradjou (1) observed no significant difference (P > 0.05) in L. monocytogenes population changes between high and low starting inoculum concentrations (7 and 5 log CFU per fruit, respectively) on peach and nectarine surfaces. L. monocytogenes populations remained unchanged on peach and nectarine surfaces for both inocula when stored at 20 and 30°C temperatures over 18 h.

DISCUSSION

Effect of surface condition

Intact produce surfaces are different, and L. monocytogenes growth is dependent on surface properties, including moisture, topography, nutrient availability, and microflora, among other factors (11, 39, 50). Growth of foodborne pathogens on intact produce surfaces is less likely to occur compared with cut produce surfaces, owing to the protective outer barriers on most intact produce (48, 88, 98, 102). The protective outer barrier of most intact produce surfaces may restrict the availability of moisture and nutrients (50). Furthermore, the chance of foodborne pathogen growth and/or survival may be increased once the protective epidermal barrier has been broken by physical damage or degradation (50). Produce that has been injured through peeling, cutting, slicing, or shredding can provide microorganisms access to nutrients and water. For example, one study (102) noted significantly reduced (P ≤ 0.05) levels of Escherichia coli O157:H7, Salmonella, and Staphylococcus over time on intact, whole apple surfaces compared with cut apple surfaces. The literature reviewed herein reported no L. monocytogenes growth on the surface of lettuce, contrasting with studies that used shredded or cut lettuce (18, 65, 84, 101). In fact, prior studies (34, 98) showed L. monocytogenes attaches preferentially to cut edges of iceberg lettuce and cut cabbage compared with intact tissues. Other pathogens including E. coli O157:H7 and Salmonella followed similar trends, with pathogen attachment more likely on injured or cut produce surfaces compared with intact produce surfaces (48, 91). Survival of microorganisms on fresh produce is affected by nutrient availability, and nutrient content has been shown to affect the growth of L. monocytogenes.

Prior studies have also investigated the association of L. monocytogenes biofilm production and nutrient availability with mixed results. Some studies (28, 58, 122) found L. monocytogenes biofilm production was enhanced in nutrient-poor environments, whereas other studies (47, 51, 94) determined L. monocytogenes biofilm production was limited in nutrient-poor environments. Those who found biofilm formation was enhanced in nutrient poor environments suggested that catabolite repression as well L. monocytogenes serotype and strain origin played a critical role (28, 58, 122). Strain-to-strain differences were also cited as influencing the ability of a given L. monocytogenes isolate to form a biofilm in nutrient-dense enviorments (94). Future studies should assess the nutrient profile and subsequent nutrient availability on the surface of whole, intact produce as predictors for L. monocytogenes growth and/or survival.

Surface topography, such as surface roughness, has also been found to influence bacterial attachment and retention to a surface (99, 115, 118). The surface topography of fruits and vegetables can be quite complex (119). For example, several studies (68, 104, 108) have hypothesized that the extensive netting on the rind or surface of cantaloupe increased adherence, biofilm formation, and growth of L. monocytogenes. A study (93) also demonstrated sanitizers were less effective against L. monocytogenes, E. coli O157:H7, and Salmonella on rough produce surfaces (lettuce and cantaloupe) compared with smooth produce surfaces (lemon, tomato, and blueberry). It is likely rougher produce surfaces may entrap microorganisms, thereby promoting pathogen survival and providing protection against potential mitigations (e.g., sanitizers). As more L. monocytogenes growth and/or survival data are generated from a variety of produce surfaces, it may be possible to classify L. monocytogenes growth and no growth on intact produce by surface topology.

The background microflora on the surface of produce has also been observed to influence L. monocytogenes survival and growth. Multiple studies (5, 39, 46, 66, 71, 73, 74) reported in this review demonstrated native microflora impacted L. monocytogenes growth and/or survival on intact produce surfaces, whereas only a few studies (13, 18, 44) reported no association between background microflora and growth of L. monocytogenes. In fact, numerous studies (6, 63, 64, 105107) have observed higher background microflora to inhibit or decrease pathogen growth rates. Both the quantity and species of background microflora may affect growth of L. monocytogenes. Pathogen populations, including L. monocytogenes on minimally processed vegetables, have been inhibited or decreased by high populations of competitive background microflora, such as lactic acid bacteria, enterobacteria, and pseudomonads (9, 17, 40, 41, 116). The ratio of native microflora to pathogens present on the surface of produce also affects the ability to inhibit or decrease L. monocytogenes. Carlin et al. (17) observed an increase in the population of L. monocytogenes on endive leaves with a reduced background microflora, indicating that background microflora could compete with L. monocytogenes for available resources. This association between high background microflora and decreased L. monocytogenes growth was also observed in two studies (73, 74) on spinach included in this review. Although the general trend of high background microflora decreasing L. monocytogenes growth is well studied, specific information on microflora type and level, among other factors, on the impact of L. monocytogenes growth and/or survival is needed.

Effect of storage temperature

The control of temperature has been used extensively throughout the food industry to limit microbial growth, improve quality, and/or extend shelf life (112, 113). Currently, the U.S. Food Code (2017) requires time and temperature control for RTE foods, including products that contain fresh produce (111). Growth of L. monocytogenes during storage has been cited as one of the main factors associated with outbreaks from RTE foods (112, 113). However, RTE foods vary in their ability to support growth of L. monocytogenes (113). For example, a study (54) observed L. monocytogenes grew significantly (P ≤ 0.05) on cut cantaloupe, honeydew, and watermelon; however, L. monocytogenes only survived on cut radish and declined on cut pineapple at 8 and 12°C for 7 days under the same conditions. The authors speculated that the high acidity (pH 3.2 to 4.0) of the pineapple may have played a role in inhibiting pathogen growth (54). L. monocytogenes growth is affected by environmental and product characteristics, such as pH, water activity, sodium chloride concentration, presence of organic acids, and background microflora. Similar to RTE foods, L. monocytogenes growth on whole, intact fruits and vegetables (i.e., raw agricultural commodities) was influenced by temperature. Whole, intact produce may be handled and stored under a wide range of temperatures (e.g., refrigerated truck, market display). L. monocytogenes can grow between −1.5 and 45°C; thus, L. monocytogenes growth and/or survival may be possible during all segments of the produce supply chain (13, 16).

Furthermore, L. monocytogenes populations grew at higher temperatures and remained stable or decreased at lower temperatures for asparagus, canary melons, cantaloupe, celery, cucumbers, mushrooms, permissions, raspberry, and spinach (8, 19, 39, 55, 65, 68, 70, 73, 74, 100, 101, 114). The combined data reported in this review suggest that storage temperature influences the growth and/or survival of L. monocytogenes on intact fruit and vegetable surfaces, with higher storage temperatures resulting in more L. monocytogenes growth. It should be noted that L. monocytogenes may still grow at refrigeration temperatures; however, data suggest a longer lag time before growth occurs (117), and several of the studies examined herein only carried experiments out to shelf time or less, allowing for the possibility of growth at refrigeration if kept beyond product shelf life. Future studies should examine L. monocytogenes growth and/or survival on intact produce at a range of temperatures found along the supply chain as well as held at a range of temperatures for shelf life, and beyond shelf life. The data generated will assist in risk modeling efforts to inform best practices because intact produce is often exposed to a range of temperatures, and product may be kept beyond the recommended shelf life.

Effect of relative humidity

Relative humidity affects the rate of water loss from plant tissues and is an important factor for the microbial quality of produce (65). The impact of relative humidity is not independent of temperature, because high relative humidity can prevent moisture loss only if the product temperature is close to the air temperature (78). Although multiple studies (1, 8, 29, 45, 55, 82) reported experimental relative humidity conditions, data were insufficient for trend identification or analysis on the effect of relative humidity on L. monocytogenes population dynamics on intact produce surfaces. In fact, only one study (65) included in this review provided an analysis of relative humidity on L. monocytogenes growth and/or survival on intact produce. L. monocytogenes populations survived better at higher relative humidity compared with L. monocytogenes populations at lower relative humidity. Furthermore, this trend was more pronounced when intact produce was stored at cooler temperatures.

Relative humidity is likely an important factor in assessing the likelihood of L. monocytogenes growth and/or survival on intact produce and may be a potential control strategy for limiting L. monocytogenes growth and/or survival on intact produce during certain activities (e.g., transportation, storage). Generally, environments with lower relative humidity may suppress L. monocytogenes growth and/or survival, especially if combined with temperature control strategies. This may be a challenge for the produce industry because relative humidity can be difficult (and potentially expensive) to control in some produce environments along the supply chain. More studies are needed to examine the impact of relative humidity on L. monocytogenes growth and/or survival on intact produce commodities (e.g., other than lettuce and cucumber). In addition, several of the published studies lacked information on relative humidity conditions; thus, future studies should include relative humidity conditions or parameters under which experiments were performed to assist in examining trends.

Effect of storage matrix

Storage containers used to hold and transport fresh produce can affect the atmosphere within the package. Similarly, respiration of produce can modify gas concentrations within the package. Modified atmosphere packaging is widely used to retard or minimize produce respiration, which can delay physiological aging and extend shelf life (39). Understanding produce respiration rates and the behaviors of gases as they relate to a storage container's permeability is important in determining L. monocytogenes growth and/or survival rates. Therefore, the storage containers used to hold and transport whole, intact produce may affect the atmosphere within the storage container. For example, modified atmospheres may naturally develop within sealed containers due to cell respiration (39). In artificial, modified atmospheres, CO2 is one primary antimicrobial factor that may inhibit or slow microorganism growth rates (79). Moreover, L. monocytogenes has shown sensitivity to CO2 in modified atmospheres (39). High CO2 concentrations may decrease pH and interfere with cell metabolism and thus may have an inhibitory effect on L. monocytogenes (31). Francis and O'Beirne (39) found that the relatively modest atmospheric changes observed in sealed polypropylene packaging film of cut lettuce and rutabaga (CO2 levels of 9 to 12% and O2 levels of 2 to 4%) did not affect the fate of L. monocytogenes, whereas the atmospheric changes in those same packages of sprouts and coleslaw did suppress L. monocytogenes growth (CO2 levels of 25 to 27% and O2 levels of 0 to 1%) (39). Vandamm et al. (114) concluded that packaging did not affect L. monocytogenes populations on celery; however, this may have been due to a low passive accumulation of CO2. Furthermore, controlled atmosphere storage of blueberries (5% O2, 15% CO2, and 80% N2) did not inhibit L. monocytogenes growth in fresh blueberries (29). Interestingly, studies (2, 10, 40) showed CO2 concentrations of 5 to 10% were not able to inhibit growth of L. monocytogenes on agar surfaces; however, CO2 concentrations of 20 and 50% were able to reduce the growth rate of L. monocytogenes, but not the maximum population density (2, 10, 40). Furthermore, Kallander et al. (59) reported that L. monocytogenes growth on shredded cabbage was not inhibited by CO2 levels up to 70%.

Results from these studies suggest that container and package material and the atmosphere created within the package or container may impact L. monocytogenes growth and/or survival on produce surfaces. Although large shifts in CO2 and O2 levels within a storage matrix may suppress L. monocytogenes growth and/or survival on produce surfaces, more research is needed because published studies are not in consensus to yield a trend for types of produce or package.

Effect of inoculation concentration

Findings from the three studies (1, 30, 38) included in this review suggest starting inoculation concentration may play a role in evaluating L. monocytogenes growth and/or survival on the intact produce surface. Lower inoculum concentrations may assist in characterizing L. monocytogenes growth potential because of carrying capacity; however, this was not the case in all studies. Each whole, intact produce commodity has its own carrying capacity, depending on factors such as background microflora and surface properties, among others (14, 42, 57, 69, 96). Thus, it is possible that L. monocytogenes behavior on intact produce surfaces in many of the studies examined in this review may have been affected by the total microbial population reaching the carrying capacity (42, 69). Dreux et al. (33) reported that three population levels (103, 107, and 108 CFU per leaf) of L. monocytogenes inoculated on parsley all had a carrying capacity of 105 CFU per leaf. The study (33) concluded that L. monocytogenes population decreases observed on parsley when the starting inoculum was higher than the carrying capacity were due to resource depletion. Bardsley et al. (8) also noted future studies should use lower starting inoculum levels (e.g., 1 to 3 log CFU per piece or g) to assist in modeling efforts by capturing growth and/or survival dynamics on produce surfaces. Other studies (42, 69) have also reported carrying capacity affecting foodborne pathogen growth and/or survival on produce surfaces. For example, Strawn and Danyluk (96) reported differences in Salmonella populations on mango and papaya as a result of the differing carrying capacities of mango versus papaya. Therefore, inoculum level (and subsequently carrying capacity) is an important factor when designing experiments and results from studies need to be in context of inoculum level.

CONCLUSIONS

This review summarizes many studies that investigated the growth and/or survival of L. monocytogenes on intact fruit and vegetable surfaces. Generally, the outer surface of fruits and vegetables was not a favorable environment for L. monocytogenes growth; however, L. monocytogenes growth and/or enhanced survival was observed under some handling and storage conditions along the supply chain. The 21 intact produce commodities examined differed in their ability to support the growth of L. monocytogenes. Data compiled from the review reported herein suggest L. monocytogenes growth and/or enhanced survival on intact fruits and vegetables was dependent on surface characteristics, temperature, relative humidity, storage matrix (e.g., package, container), and starting inoculum concentration. Identification of these factors that influence the growth and/or enhanced survival of L. monocytogenes on intact produce will assist the industry in identifying L. monocytogenes contamination risk (by adopting best practices or implementing mitigations specific to the handling, transporting, storing, and displaying of their specific commodities). The review also emphasized future studies describing experimental conditions, such as relative humidity, that may have useful applications for risk modeling or comparison studies of L. monocytogenes on intact produce.

ACKNOWLEDGMENTS

This project was funded, in part, by the Specialty Crop Block Grant Program at the USDA through the Texas Department of Agriculture and by the Center for Produce Safety. Funding for this work was also provided by the Virginia Agricultural Experiment Station and the Hatch Program of the National Institute of Food and Agriculture, USDA. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the USDA.

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