Next Article in Journal
Meropenem MICs at Standard and High Inocula and Mutant Prevention Concentration Inter-Relations: Comparative Study with Non-Carbapenemase-Producing and OXA-48-, KPC- and NDM-Producing Klebsiella pneumoniae
Next Article in Special Issue
Shotgun Metagenomics-Guided Prediction Reveals the Metal Tolerance and Antibiotic Resistance of Microbes in Poly-Extreme Environments in the Danakil Depression, Afar Region
Previous Article in Journal
Beta-Lactam Dose Optimisation in the Intensive Care Unit: Targets, Therapeutic Drug Monitoring and Toxicity
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Antibiotics
Volume 12
Issue 5
10.3390/antibiotics12050871
antibiotics-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

ESKAPEE Pathogen Biofilm Control on Surfaces with Probiotic Lactobacillaceae and Bacillus species

by
Claudio Neidhöfer
1,*,
Kamni Rathore
1,2,
Marijo Parčina
1 and
Martin A. Sieber
2
1
Institute of Medical Microbiology, Immunology and Parasitology, University Hospital Bonn, Venusberg-Campus 1, 53127 Bonn, Germany
2
Institute for Functional Gene Analytics, Bonn-Rhein-Sieg University of Applied Sciences, 53757 Sankt Augustin, Germany
*
Author to whom correspondence should be addressed.
Antibiotics 2023, 12(5), 871; https://doi.org/10.3390/antibiotics12050871
Submission received: 24 March 2023 / Revised: 21 April 2023 / Accepted: 5 May 2023 / Published: 8 May 2023
(This article belongs to the Special Issue Microbiome-Based Therapies: Alternatives to, Complementing or Enhancing Antibiotic Treatments)
Browse Figure
Versions Notes

Abstract

:
Combatting the rapidly growing threat of antimicrobial resistance and reducing prevalence and transmission of ESKAPEE pathogens in healthcare settings requires innovative strategies, one of which is displacing these pathogens using beneficial microorganisms. Our review comprehensively examines the evidence of probiotic bacteria displacing ESKAPEE pathogens, with a focus on inanimate surfaces. A systematic search was conducted using the PubMed and Web of Science databases on 21 December 2021, and 143 studies were identified examining the effects of Lactobacillaceae and Bacillus spp. cells and products on the growth, colonization, and survival of ESKAPEE pathogens. While the diversity of study methods limits evidence analysis, results presented by narrative synthesis demonstrate that several species have the potential as cells or their products or supernatants to displace nosocomial infection-causing organisms in a variety of in vitro and in vivo settings. Our review aims to aid the development of new promising approaches to control pathogen biofilms in medical settings by informing researchers and policymakers about the potential of probiotics to combat nosocomial infections. More targeted studies are needed to assess safety and efficacy of different probiotic formulations, followed by large-scale studies to assess utility in infection control and medical practice.

1. Introduction

Antimicrobial resistance (AMR) is a major global health threat, resulting in millions of deaths each year from antibiotic-resistant infections [1,2]. The most common causes of these infections are a group of bacteria known as ESKAPEE pathogens (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumonia, Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter species, and Escherichia coli). As patients with weakened immune systems and antibiotic-induced dysbiosis are at increased risk of developing these infections, hospitals are particularly vulnerable to the spread of ESKAPEE pathogens [3,4]. Reducing the transmission of these infections in hospitals is critical to addressing the overall public health threat posed by AMR [3,5,6].
To reduce the risk of hospital-acquired infections (HAIs) in hospitals and other healthcare facilities, commonly, disinfectants are used. However, the overuse and improper use of disinfectants favor the development and spread of AMR organisms through the selection pressure exerted on microbial populations [7,8,9,10,11]. The reduction in susceptible microorganisms facilitates multiplication and overgrowth of the resistant ones. In addition, the widespread use of disinfectants can also lead to the emergence of cross-resistance [12,13].
In recent years, there has been interest in using probiotic-based cleaning formulations as alternative cleaning agents in hospitals and other healthcare settings [8,10,11,14,15,16,17,18]. Unlike traditional disinfectants, which unselectively eliminate microorganisms, probiotics used in this context are more selective and might only target specific microorganisms by directly eliminating or suppressing growth. This means that they are less likely to lead to the development of AMR strains of bacteria. There is some evidence to suggest that probiotic-based cleaning formulations may be effective at reducing the risk of HAIs in hospitals [8,14,15,16]. However, more research is needed to confirm the effectiveness of probiotics as a standalone cleaning agent in the hospital setting. The effectiveness of probiotics in reducing the risk of HAIs depends on various factors, including the specific strain or strains of bacteria used, the dose and mode of application of the probiotic, and the patient population under study.
In-depth analysis is needed to identify which specific probiotic bacterial strains are most effective in reducing the risk of hospital-acquired infections. While Lactobacillaceae and Bacilli have demonstrated their potential in some studies, it is crucial to consider the unique properties of different probiotic strains and the specific conditions in which they are used. It is also essential to consider the ways in which probiotic strains may interact with each other, conventional antimicrobials, and the potential for adverse effects in certain patient populations. In this review, we focus on the effect of probiotic Lactobacillaceae and Bacilli as well as their products in the direct and indirect elimination of ESKAPEE pathogens.

2. Results

2.1. Species Reported to Suppress ESKAPEE Pathogen Growth

Among Lactobacillaceae, Lactiplantibacillus plantarum was the most frequently reported species, with 36 instances of growth inhibiting, bactericidal, or anti-biofilm properties against at least one ESKAPEE pathogen [19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54]. Lactobacillus fermentum [21,22,28,30,31,43,55,56,57,58,59,60,61,62,63,64,65] and Lacticaseibacillus rhamnosus [19,21,25,27,31,66,67,68,69,70,71,72,73,74,75,76,77] were both reported 17 times, Lactobacillus acidophilus was reported 16 times [21,28,55,67,78,79,80,81,82,83,84,85,86,87,88,89]. The next most common species were Lactobacillus paracasei (11 times) [19,20,58,73,74,77,90,91,92,93,94], Lactobacillus casei (9 times) [88,95,96,97,98,99,100,101,102], Limosilactobacillus reuteri (6 times) [19,103,104,105,106,107], Levilactobacillus brevis (6 times) [19,25,29,108,109,110], Lactobacillus salivarius [50,111,112,113] and Lactobacillus helveticus [40,102,114,115] (4 times), Lactobacillus delbrueckii [19,116,117] and Lactobacillus crispatus [65,118,119] (3 times), Lactobacillus pentosus [26,120], Lactobacillus gasseri [119,121], and Lactobacillus curvatus [51,102] (2 times). Lactobacillus agilis [122], Lactobacillus caucasicus [19], Lactobacillus gallinarum [31], Lactobacillus gastricus [90], Lactobacillus johnsonii [24], Lactobacillus kunkeei [123], Lactobacillus murinus [124], Latilactobacillus sakei [102], Lactobacillus vaginalis [106] and Lacticaseibacillus zeae [58] were each only reported once. Among Bacilli, Bacillus subtilis was the most frequently reported species (five times) [125,126,127,128,129], followed by Bacillus velezensis (two times) [130,131]. Bacillus thuringiensis [46], Bacillus amyloliquefaciens [126], Bacillus cereus [132] and Bacillus pumilus [133] were each reported once.

2.2. Origin of the Isolates

Among cases where information on the origin of the isolates was provided, probiotic bacteria were most frequently isolated from more and less fermented food (22 times) [20,22,26,41,43,44,45,48,49,74,95,102,107,109,110,128,134,135,136,137,138,139] and dairy products (11 times) [24,31,40,57,58,69,79,86,90,97,108,117]. Some were of human origin; these included bacteria of vaginal origin (six times) [64,65,72,93,119,140], such isolated from infant GI-tracts (six times) [24,42,62,77,94], and bacteria from the oral cavity (three times) [56,58,78], intestine (two times) [59,141] and one from breastmilk [75]. Others were of animal origin; these included three of bovine origin [25,29,33], two isolated from pigs [122,142], two from bees [123,131], and one from poultry [106], a dog [124], a bullfrog [51] and camel milk [23], respectively. Two Bacillus isolates were of marine origin [127,133]. Information on the origin of the remaining isolates was either not available or they were derived from probiotic bacteria-based products or microbiological strain collections.

2.3. Nature of Conducted Experiments

The vast majority of studies were based on in vitro experiments (132 times) in which the effects of probiotic bacteria against pathogens were mainly evaluated by agar spot tests, agar well tests, co-culture in liquid media and on the surface of human cell lines. The latter included Caco-2 [44,50,89,103], HT29 [24,89,101], HeLa 229 [65,83], vaginal epithelial cells [71], and uroepithelial cells [143]. Some of the in vitro experiments tested the anti-biofilm properties of the probiotic bacteria on inert surfaces [81,93,125], most importantly on metals such as stainless steel [120] or titanium [28]. Other surfaces included those made of silicon [32], ceramics, and linoleum [144]. Six studies were based exclusively on in vivo experiments. These included three rat disease models, two of which were for wounds [53,54] and one was for surgical implants [55], two murine disease models [145], one of which also included a bovine disease model [130], one rabbit model knee implant infection [76] and one bee model [123]. Three studies were based on combined in vitro and in vivo experiments and exclusively included murine disease models, two intestinal colonization models [36,52] and one urinary tract infection model [113]. In one of the latter, the anti-pathogenic properties demonstrated in vitro could not be replicated in vivo [52].

2.4. Suppression of ESKAPEE Pathogens

The ESKAPEE pathogens that were most frequently reported to be displaced by the probiotic bacteria were by far Staphylococcus aureus (77 times) and Escherichia coli (73 times). The next most common ESKAPEE pathogen to be described as having been displaced was Pseudomonas aeruginosa (30 times). These three were also by far the most frequently tested ESKAPEE pathogens. Table 1 displays the number of times each probiotic species was reported to displace these three pathogens. Less frequently tested and displaced were Klebsiella pneumoniae (nine times) [26,43,52,56,65,79,132,136,146], Enterococci (five times) [85,103,107,141,147], Enterobacter species (two times) [26,61] and Acinetobacter baumannii (once) [68]. Of the Enterococcus isolates, four were E. faecalis and one E. faecium. Nine reports described pathogen inhibition to be caused by direct competition between probiotic and pathogenic bacterial cells [24,29,32,40,102,108,135,143,148]. Nineteen studies pinned the bactericidal properties down on one or more specific cell products [46,49,51,56,57,59,73,76,99,100,117,125,127,129,133,136,149,150,151]. Eleven studies ascribed the suppression of pathogens to be attributable to both, direct competition and cell products [27,55,61,64,72,75,77,104,116,126,152]. Five studies linked attributed bactericidal activity exclusively to lactic acid and pH reduction [98,119,137,138,153]. The remaining 52 studies that identified the inhibition mechanism narrowed it down to be the cell-free supernatant (CFS) or exclusively investigated the CFS of probiotic bacteria. Nigatu and Gashe (1994) reported inhibitory effects to be independent of pH [136], Kang et al. (2017) discovered that pH neutralized CFS was still efficient in killing pathogenic bacteria as long as it was not heat inactivated or proteinase K treated [111]. Jeyanathan et al. (2021) described whole cell cultures to be ineffective in preventing P. aeruginosa growth, while CFS significantly reduced adherence and viability [28].
Twenty-four studies described tested probiotic bacteria as having significant anti-biofilm properties. These biofilms were of S. aureus (14 reports) [22,24,25,42,59,68,81,88,95,107,108,114,130,154], E. coli (9 reports) [24,26,60,68,70,95,101,152,154], P. aeruginosa (7 reports) [26,42,59,113,123,153,155], K. pneumoniae (2 reports) [26,146], E. faecalis (1 report) [107], Enterobacter (1 report) [26] and A. baumannii (1 report) [68] isolates. Biofilm impairment was generally by co-aggregation [24,81,108], by reducing pathogen adhesion [42,60,68,101,114], or by disrupting cell metabolism or interfering with quorum sensing [46,70]. Chappell and Nair (2020) determined P. aeruginosa inhibition to be dependent on pH reduction [153]. Koohestani et al. (2018) discovered Lact. acidophilus CFS to better remove S. aureus biofilms than Lact. casei CFS [88]. Five authors reported the probiotic bacteria capable of replacing the pathogens’ biofilms with their own, which subsequently prevented recolonization by the pathogenic species [25,60,68,123,152]. Several additional studies reported the ability of pathogens to adhere and survive on probiotic-covered surfaces or such covered with probiotic-products to be significantly reduced [27,30,32,37,55,102,125,135,144,156]. Kheiri et al. (2020) discovered Lactobacillus CFSs, even in 1:16 dilutions, to have superior biofilm-inhibiting and -killing properties than supra-MIC levels of several tested antibiotics [146].
Among studies evaluating the activity of probiotic bacteria or their products against S. aureus, eight included methicillin-resistant S. aureus (MRSA) strains [21,53,75,121,126,127,131,151]. Kalayci Yüksek et al. (2021) detected low protective effect of Lact. acidophilus, Lact. plantarum, Lact. fermentum and Lact. rhamnosus on MRSA [21]; Sürmeli et al. (2019) detected no therapeutic effect but good protective effect of Lact. plantarum in preventing MRSA colonization when applied before MRSA on wounds [53]. Algburi et al. (2021) determined CFS of B. subtilis and B. amyloliquefaciens to inhibit both MRSA and methicillin-susceptible S. aureus (MSSA) [126]. Liu et al. (2020) reported also Lact. rhamnosus to inhibit both MSSA and MRSA in vitro and in the murine model [75]. Kalpana et al. (2012) described the products of B. subtilis to inhibit MRSA but not P. aeruginosa [127]. Klimko et al. (2020) discovered Lact. acidophilus to be the strongest S. aureus inhibitor among nine tested probiotic isolates [19].
Two studies evaluating the activity of probiotic bacteria or their products against E. coli included enterohemorrhagic (EHEC) strains [96,135], two included enteropathogenic EPEC strains [36,89], and one contained an extended-spectrum beta-lactamase-encoding E. coli [79]. All reported the tested Lactobacillales to displace the pathogens. Six studies included not only ESKAPEE pathogens but also other Enterobacterales that frequently cause HAIs, such as Proteus mirabilis [61,65,157] and Proteus vulgaris [51], Klebsiella oxytoca [61] and Klebsiella aerogenes [129], Citrobacter freundii [51,61], and Serratia marcescens [140] to be inhibited by probiotic bacteria. Scillato et al. (2021) reported Lact. fermentum and Lact. crispatus to displace P. mirabilis and even KPC carbapenemase-encoding K. pneumoniae, but not E. faecalis, vancomycin-resistant E. faecium, or Candida albicans [65]. In the meantime, Strus et al. (2020) only discovered a few lactobacilli able to inhibit E. faecalis [158]. De Souza Freitas et al. (2020) determined B. subtilis CFS to also inhibit less frequent nonfermenting HAI-causing pathogens Achromobacter xylosoxidans, Alcaligenes faecalis, and Pseudomonas alcaligenes [129]. Turkova et al. (2013) reported Lact. acidophilus, Lact. gasseri, and Lact. helveticus to inhibit E. coli, E. faecalis and even Clostridioides difficile, while S. aureus was not inhibited by Lact. Helveticus [147]. One study reported some Lactobacillales to enhance E. coli growth [33].

3. Discussion

The protective effects of colonizing the human body [159,160,161,162,163,164,165] or food [159,166,167] with probiotics have been well studied. However, applying this concept to infection vector-transmitting surfaces such as those found in hospitals through protective probiotic films is a novel approach that challenges traditional infection prevention strategies centered on maintaining a sterile hospital environment. Probiotic cleaning formulations show promise as a potential solution to the proliferation of antimicrobial resistance, particularly in healthcare settings [8,10,11,14,15,16,17]. These products, which contain live microorganisms beneficial to the cleaned environment, may restore microbial balance and reduce selective pressure driving drug-resistant bacteria. They may also have a more favorable environmental profile due to their use of natural, biodegradable ingredients.
Our review of the efficacy of probiotics in reducing the presence of ESKAPEE pathogens identified numerous studies that analyzed the bactericidal properties of probiotic strains against E. coli and S. aureus, which are well-known causes of gastroenteritis [168] particularly relevant to the use of probiotics in the gastrointestinal tract. The probiotic isolates examined in these studies were primarily Lactobacilli, aligning with the focus on using probiotics in the gut. In addition, most studies simulated conditions present in the gastrointestinal tract. P. aeruginosa, a microorganism known to cause food spoilage [169], was also frequently examined for its susceptibility to probiotics. However, there were very few studies that investigated the effects of probiotics against the majority of other ESKAPEE pathogens.
It is important to note that the greater number of studies demonstrating the bactericidal effects of Lactobacillales does not necessarily indicate superior performance in suppressing ESKAPEE pathogens compared to Bacillus species. Rather, evaluating probiotics for use on hospital surfaces requires a more nuanced analysis that considers factors such as survivability, biofilm formation, and bactericidal activity at room temperature and under nutrient-poor conditions, which may instead make Bacillus species more attractive candidates. It is also crucial to recognize that significant strain-level variations within the same species can impact the desired properties [170,171].
Despite the generally recognized safety of probiotics and the fact that most were derived from benign edible sources some of which are even consumed in large quantities, the use of these microorganisms in hospitals warrants further investigation to ensure their safety, particularly in dysbiotic, immunocompromised, leukopenic or even agranulocytic patients [172,173,174,175], as these are patient groups that could particularly benefit from such innovative solutions [176,177,178,179,180,181,182,183,184]. It is desirable for these microorganisms, which may be transferred from the environment to the patient, to retain their protective effects in the patient as well.
Conducting more targeted studies on hospital or similar surfaces and the specific pathogens to be displaced provide valuable insights and aid in the development of new and promising approaches for preventing or eradicating bacterial biofilms in medical settings [185,186,187]. Comparison of different probiotic-based cleansing formulations should also be considered, as the efficacy or inefficacy of one product may not necessarily apply to other products with different strains.

4. Materials and Methods

A systematic search was conducted using the PubMed and Web of Science databases. The search was performed on 21 December 2021. The search string used was the following:
“(Probiotic-Based Cleaning OR Antagonistic Activit* OR Inhibition OR Disinfectant OR Anti-infective OR Biofilm removal OR cleaning solution* OR infection control OR antibiofilm OR biosurfactants OR Sanitation OR Surfactants OR Cleaning OR Bacteriostatic OR Antimicrobial OR Microbial based cleaning OR Antagonistic activity OR Lantibiotics OR bacteriocins OR antagonistic activity) AND (biofilm OR Surface OR medical device) AND (Staphylococcus aureus OR Klebsiella pneumoniae OR Acinetobacter baumannii OR Pseudomonas aeruginosa OR E. coli OR Enterobac* OR Nonfermen* OR MRSA OR CRE OR MDR) AND (Lactobacill* OR Probiotics OR Bacillus OR Clostridi* OR Bacteroi*) NOT “Review” [pt]”.
For the assessment of search results, results were imported into CITAVI Database. Two reviewers independently screened the titles and abstracts of the identified studies for eligibility. Studies were eligible for inclusion if they examined the effects of Lactobacillus, Lacticaseibacillus, Lactiplantibacillus, Limosilactobacillus, Latilactobacillus or Bacillus spp. or their products/supernatants on one or more ESKAPEE pathogens. ESKAPEE pathogens were defined as Enterococcus faecalis, Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter species, and Escherichia coli. Full-text articles were then obtained for all potentially eligible studies and assessed for inclusion based on the predefined inclusion and exclusion criteria. Any discrepancies between the reviewers were resolved through discussion and consensus.
Overall, a total of 143 studies were included in the review (see Figure 1). The studies were conducted in a variety of settings and involved a range of bacterial strains and ESKAPEE pathogens. The experiments included both in vitro and in vivo studies, and a variety of methods were used to assess the effects of the probiotic bacteria on the growth, colonization, and survival of the pathogens.
Data were extracted from the included studies using a standardized data extraction form. The following data were extracted: examined bacteria, ESKAPEE pathogens they were tested against, environment tested in, type of experiment, and, if applicable, additional relevant information. The extracted data were synthesized and analyzed using a narrative synthesis approach. The results were organized by bacteria and pathogens tested and summarized in a tabular format.
Our review aimed to provide a comprehensive overview of the available evidence on the effects of Lactobacilli and Bacilli or their products against ESKAPEE pathogens. By synthesizing and analysing the data from the included studies, we aimed to evaluate the potential of these probiotic bacteria as means to combat infections caused by these pathogens.

5. Conclusions

The evidence collected from the multitude of scientific studies shows that many Lactobacillaceae and Bacillus species are able to suppress the proliferation of ESKAPEE pathogens. However, the experimental conditions under which these studies were conducted do not allow conclusive assessments of the efficacy of the species in protecting hospital surfaces, which could contribute to the development of new promising approaches to prevent or eradicate bacterial biofilms in medical settings. More targeted studies on hospital surfaces and pathogens to be displaced are needed to understand the potential of each species and strain in more detail, along with their respective safety profiles. Once a safe and effective formulation is identified, conducting large-scale studies seems imperative, given the potential they carry in tackling several issues infection control and medical practice in general are currently facing.

Author Contributions

Conceptualization, C.N. and M.A.S.; methodology, C.N. and M.A.S.; software, C.N. and M.A.S.; validation, C.N. and M.A.S.; formal analysis, C.N. and M.A.S.; investigation, C.N., K.R. and M.A.S.; resources, M.P. and M.A.S.; data curation, C.N., K.R. and M.A.S.; writing—original draft preparation, C.N. and K.R.; writing—review and editing, C.N., M.P. and M.A.S.; visualization, C.N. and M.A.S.; supervision, C.N., M.P. and M.A.S.; project administration, C.N. and M.A.S.; funding acquisition, M.P. and M.A.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Prestinaci, F.; Pezzotti, P.; Pantosti, A. Antimicrobial resistance: A global multifaceted phenomenon. Pathog. Glob. Health 2015, 109, 309–318. [Google Scholar] [CrossRef] [PubMed]
  2. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet 2022, 399, 629–655. [Google Scholar] [CrossRef] [PubMed]
  3. Blake, K.S.; Choi, J.; Dantas, G. Approaches for characterizing and tracking hospital-associated multidrug-resistant bacteria. Cell. Mol. Life Sci. 2021, 78, 2585–2606. [Google Scholar] [CrossRef]
  4. Salmanov, A.; Shchehlov, D.; Svyrydiuk, O.; Bortnik, I.; Mamonova, M.; Korniyenko, S.; Rud, V.; Artyomenko, V.; Gudym, M.; Maliarchuk, R.; et al. Epidemiology of healthcare-associated infections and mechanisms of antimicrobial resistance of responsible pathogens in Ukraine: A multicentre study. J. Hosp. Infect. 2022, 131, 129–138. [Google Scholar] [CrossRef] [PubMed]
  5. Stewart, S.; Robertson, C.; Pan, J.; Kennedy, S.; Haahr, L.; Manoukian, S.; Mason, H.; Kavanagh, K.; Graves, N.; Dancer, S.; et al. Impact of healthcare-associated infection on length of stay. J. Hosp. Infect. 2021, 114, 23–31. [Google Scholar] [CrossRef]
  6. Majumder MA, A.; Rahman, S.; Cohall, D.; Bharatha, A.; Singh, K.; Haque, M.; Gittens-St Hilaire, M. Antimicrobial Stewardship: Fighting Antimicrobial Resistance and Protecting Global Public Health. Infect. Drug Resist. 2020, 13, 4713–4738. [Google Scholar] [CrossRef]
  7. Kraemer, S.A.; Ramachandran, A.; Perron, G.G. Antibiotic Pollution in the Environment: From Microbial Ecology to Public Policy. Microorganisms 2019, 7, 180. [Google Scholar] [CrossRef] [PubMed]
  8. Caselli, E.; D’accolti, M.; Soffritti, I.; Lanzoni, L.; Bisi, M.; Volta, A.; Berloco, F.; Mazzacane, S. An Innovative Strategy for the Effective Reduction of MDR Pathogens from the Nosocomial Environment. Adv. Exp. Med. Biol. 2019, 1214, 79–91. [Google Scholar] [CrossRef]
  9. Raymond, B. Five rules for resistance management in the antibiotic apocalypse, a road map for integrated microbial management. Evol. Appl. 2019, 12, 1079–1091. [Google Scholar] [CrossRef]
  10. Velazquez, S.; Griffiths, W.; Dietz, L.; Horve, P.; Nunez, S.; Hu, J.; Shen, J.; Fretz, M.; Bi, C.; Xu, Y.; et al. From one species to another: A review on the interaction between chemistry and microbiology in relation to cleaning in the built environment. Indoor Air 2019, 29, 880–894. [Google Scholar] [CrossRef]
  11. Scott, E.A.; Bruning, E.; Nims, R.W.; Rubino, J.R.; Ijaz, M.K. A 21st century view of infection control in everyday settings: Moving from the Germ Theory of Disease to the Microbial Theory of Health. Am. J. Infect. Control 2020, 48, 1387–1392. [Google Scholar] [CrossRef] [PubMed]
  12. Pereira, B.M.P.; Wang, X.; Tagkopoulos, I. Biocide-Induced Emergence of Antibiotic Resistance in Escherichia coli. Front. Microbiol. 2021, 12, 640923. [Google Scholar] [CrossRef]
  13. Fernandes, P.; Ferreira, B.S.; Cabral, J.M.S. Solvent tolerance in bacteria: Role of efflux pumps and cross-resistance with antibiotics. Int. J. Antimicrob. Agents 2003, 22, 211–216. [Google Scholar] [CrossRef] [PubMed]
  14. Caselli, E.; Arnoldo, L.; Rognoni, C.; D’Accolti, M.; Soffritti, I.; Lanzoni, L.; Bisi, M.; Volta, A.; Tarricone, R.; Brusaferro, S.; et al. Impact of a probiotic-based hospital sanitation on antimicrobial resistance and HAI-associated antimicrobial consumption and costs: A multicenter study. Infect. Drug Resist. 2019, 12, 501–510. [Google Scholar] [CrossRef] [PubMed]
  15. Vandini, A.; Temmerman, R.; Frabetti, A.; Caselli, E.; Antonioli, P.; Balboni, P.G.; Platano, D.; Branchini, A.; Mazzacane, S. Hard Surface Biocontrol in Hospitals Using Microbial-Based Cleaning Products. PLoS ONE 2014, 9, e108598. [Google Scholar] [CrossRef]
  16. Caselli, E.; D’accolti, M.; Vandini, A.; Lanzoni, L.; Camerada, M.T.; Coccagna, M.; Branchini, A.; Antonioli, P.; Balboni, P.G.; Di Luca, D.; et al. Impact of a Probiotic-Based Cleaning Intervention on the Microbiota Ecosystem of the Hospital Surfaces: Focus on the Resistome Remodulation. PLoS ONE 2016, 11, e0148857. [Google Scholar] [CrossRef]
  17. Gebrayel, P.; Nicco, C.; Al Khodor, S.; Bilinski, J.; Caselli, E.; Comelli, E.M.; Egert, M.; Giaroni, C.; Karpinski, T.M.; Loniewski, I.; et al. Microbiota medicine: Towards clinical revolution. J. Transl. Med. 2022, 20, 111. [Google Scholar] [CrossRef]
  18. Erem, A.D.; Wessman, P.; Husmark, U.; Nierstrasz, V. Biocontrol of solid surfaces in hospitals using microbial-based wipes. Text. Res. J. 2017, 89, 216–222. [Google Scholar] [CrossRef]
  19. Klimko, A.I.; Cherdyntseva, T.A.; Brioukhanov, A.L.; Netrusov, A.I. In Vitro Evaluation of Probiotic Potential of Selected Lactic Acid Bacteria Strains. Probiotics Antimicrob. Proteins 2020, 12, 1139–1148. [Google Scholar] [CrossRef]
  20. Jia, G.; Liu, X.; Zhi, A.; Li, J.; Wu, Y.; Zhang, Y. Characterization and Selection of Lactobacillus plantarum and Lactobacillus paracasei for prevention of oral bacterial infections from Chinese pickle. AMB Express 2021, 11, 84. [Google Scholar] [CrossRef]
  21. Kalaycı Yüksek, F.; Gümüş, D.; Gündoğan, G.İ.; Anğ Küçüker, M. Cell-Free Lactobacillus Sp. Supernatants Modulate Staphylococcus aureus Growth, Adhesion and Invasion to Human Osteoblast (HOB) Cells. Curr. Microbiol. 2021, 78, 125–132. [Google Scholar] [PubMed]
  22. Melo, T.A.; dos Santos, T.F.; de Almeida, M.E.; Junior, L.A.G.F.; Andrade, E.F.; Rezende, R.P.; Marques, L.M.; Romano, C.C. Inhibition of Staphylococcus aureus biofilm by Lactobacillus isolated from fine cocoa. BMC Microbiol. 2016, 16, 250. [Google Scholar] [CrossRef] [PubMed]
  23. Sharma, A.; Lavania, M.; Singh, R.; Lal, B. Identification and probiotic potential of lactic acid bacteria from camel milk. Saudi J. Biol. Sci. 2021, 28, 1622–1632. [Google Scholar] [CrossRef] [PubMed]
  24. Vizoso Pinto, M.G.; Schuster, T.; Briviba, K.; Watzl, B.; Holzapfel, W.H.; Franz, C.M. Adhesive and Chemokine Stimulatory Properties of Potentially Probiotic Lactobacillus Strains. J. Food Prot. 2007, 70, 125–134. [Google Scholar]
  25. Wallis, J.K.; Krömker, V.; Paduch, J.-H. Biofilm Challenge: Lactic Acid Bacteria Isolated from Bovine Udders versus Staphylococci. Foods 2019, 8, 79. [Google Scholar] [CrossRef] [PubMed]
  26. Rao, K.P.; Chennappa, G.; Suraj, U.; Nagaraja, H.; Raj, A.P.C.; Sreenivasa, M.Y. Probiotic Potential of Lactobacillus Strains Isolated from Sorghum-Based Traditional Fermented Food. Probiotics Antimicrob. Proteins 2015, 7, 146–156. [Google Scholar] [CrossRef]
  27. Rezaei, Z.; Khanzadi, S.; Salari, A. Biofilm formation and antagonistic activity of Lacticaseibacillus rhamnosus (PTCC1712) and Lactiplantibacillus plantarum (PTCC1745). AMB Express 2021, 11, 156. [Google Scholar] [CrossRef]
  28. Jeyanathan, A.; Ramalhete, R.; Blunn, G.; Gibbs, H.; Pumilia, C.A.; Meckmongkol, T.; Lovejoy, J.; Coathup, M.J. Lactobacillus cell-free supernatant as a novel bioagent and biosurfactant against Pseudomonas aeruginosa in the prevention and treatment of orthopedic implant infection. J. Biomed. Mater. Res. B Appl. Biomater. 2021, 109, 1634–1643. [Google Scholar]
  29. Bouchard, D.S.; Seridan, B.; Saraoui, T.; Rault, L.; Germon, P.; Moreno, C.G.; Nader-Macias, F.M.E.; Baud, D.; Francois, P.; Chuat, V.; et al. Lactic Acid Bacteria Isolated from Bovine Mammary Microbiota: Potential Allies against Bovine Mastitis. PLoS ONE 2015, 10, e0144831. [Google Scholar] [CrossRef]
  30. Nataraj, B.H.; Ramesh, C.; Mallappa, R.H. Functional group characterization of lactic bacterial biosurfactants and evaluation of antagonistic actions against clinical isolates of methicillin-resistant Staphylococcus aureus. Lett. Appl. Microbiol. 2021, 73, 372–382. [Google Scholar] [CrossRef] [PubMed]
  31. Bujňáková, D.; Kmet, V. Functional properties of Lactobacillus strains isolated from dairy products. Folia Microbiol. 2012, 57, 263–267. [Google Scholar] [CrossRef] [PubMed]
  32. Carvalho, F.M.; Teixeira-Santos, R.; Mergulhão, F.J.M.; Gomes, L.C. Effect of Lactobacillus plantarum Biofilms on the Adhesion of Escherichia coli to Urinary Tract Devices. Antibiotics 2021, 10, 966. [Google Scholar] [CrossRef] [PubMed]
  33. Rodriguez-Palacios, A.; Staempfli, H.R.; Duffield, T.; Weese, J.S. Isolation of bovine intestinal Lactobacillus plantarum and Pediococcus acidilactici with inhibitory activity against Escherichia coli O157 and F5. J. Appl. Microbiol. 2009, 106, 393–401. [Google Scholar] [PubMed]
  34. Zdenkova, K.; Alibayov, B.; Karamonova, L.; Purkrtova, S.; Karpiskova, R.; Demnerova, K. Transcriptomic and metabolic responses of Staphylococcus aureus in mixed culture with Lactobacillus plantarum, Streptococcus thermophilus and Enterococcus durans in milk. J. Ind. Microbiol. Biotechnol. 2016, 43, 1237–1247. [Google Scholar]
  35. Danilova, T.A.; Adzhieva, A.A.; Danilina, G.A.; Polyakov, N.B.; Soloviev, A.I.; Zhukhovitsky, V.G. Antimicrobial Activity of Supernatant of Lactobacillus plantarum against Pathogenic Microorganisms. Bull. Exp. Biol. Med. 2019, 167, 751–754. [Google Scholar] [CrossRef]
  36. Liu, Z.; Ma, Y.; Yang, J.; Zhang, P.; Moyer, M.P.; Qin, H. Expression of the Lactobacillus plantarum Surface Layer MIMP Protein Protected NCM460 Epithelial Cells from Enteroinvasive Escherichia coli Infection. Cell. Physiol. Biochem. 2011, 27, 99–108. [Google Scholar]
  37. Ramos, A.N.; Sesto Cabral, M.E.; Noseda, D.; Bosch, A.; Yantorno, O.M.; Valdez, J.C. Antipathogenic properties of Lactobacillus plantarum on Pseudomonas aeruginosa: The potential use of its supernatants in the treatment of infected chronic wounds. Wound Repair Regen. 2012, 20, 552–562. [Google Scholar] [CrossRef]
  38. Yan, X.; Gu, S.; Cui, X.; Shi, Y.; Wen, S.; Chen, H.; Ge, J. Antimicrobial, anti-adhesive and anti-biofilm potential of biosurfactants isolated from Pediococcus acidilactici and Lactobacillus plantarum against Staphylococcus aureus CMCC26003. Microb. Pathog. 2019, 127, 12–20. [Google Scholar] [CrossRef]
  39. Apiwatsiri, P.; Pupa, P.; Yindee, J.; Niyomtham, W.; Sirichokchatchawan, W.; Lugsomya, K.; Shah, A.A.; Prapasarakul, N. Anticonjugation and Antibiofilm Evaluation of Probiotic Strains Lactobacillus plantarum 22F, 25F, and Pediococcus acidilactici 72N Against Escherichia coli Harboring mcr-1 Gene. Front. Veter-Sci. 2021, 8, 614439. [Google Scholar] [CrossRef]
  40. Cui, X.; Shi, Y.; Gu, S.; Yan, X.; Chen, H.; Ge, J. Antibacterial and Antibiofilm Activity of Lactic Acid Bacteria Isolated from Traditional Artisanal Milk Cheese from Northeast China Against Enteropathogenic Bacteria. Probiotics Antimicrob. Proteins 2018, 10, 601–610. [Google Scholar] [CrossRef]
  41. Das, D.; Goyal, A. Potential probiotic attributes and antagonistic activity of an indigenous isolate Lactobacillus plantarum DM5 from an ethnic fermented beverage “Marcha” of North Eastern Himalayas. Int. J. Food Sci. Nutr. 2014, 65, 335–344. [Google Scholar] [CrossRef] [PubMed]
  42. Onbas, T.; Osmanagaoglu, O.; Kiran, F. Potential Properties of Lactobacillus plantarum F-10 as a Bio-control Strategy for Wound Infections. Probiotics Antimicrob. Proteins 2019, 11, 1110–1123. [Google Scholar] [CrossRef] [PubMed]
  43. Von Mollendorff, J.W.; Todorov, S.; Dicks, L.M.T. Comparison of Bacteriocins Produced by Lactic-Acid Bacteria Isolated from Boza, a Cereal-Based Fermented Beverage from the Balkan Peninsula. Curr. Microbiol. 2006, 53, 209–216. [Google Scholar] [CrossRef] [PubMed]
  44. Lee, J.-E.; Lee, N.-K.; Paik, H.-D. Antimicrobial and anti-biofilm effects of probiotic Lactobacillus plantarum KU200656 isolated from kimchi. Food Sci. Biotechnol. 2021, 30, 97–106. [Google Scholar] [CrossRef] [PubMed]
  45. Gupta, A.; Tiwari, S.K. Probiotic Potential of Lactobacillus plantarum LD1 Isolated from Batter of Dosa, a South Indian Fermented Food. Probiotics Antimicrob. Proteins 2014, 6, 73–81. [Google Scholar] [CrossRef] [PubMed]
  46. Joshi, S.; Kaur, A.; Sharma, P.; Harjai, K.; Capalash, N. Lactonase-expressing Lactobacillus plantarum NC8 attenuates the virulence factors of multiple drug resistant Pseudomonas aeruginosa in co-culturing environment. World J. Microbiol. Biotechnol. 2014, 30, 2241–2249. [Google Scholar] [CrossRef]
  47. Mohapatra, A.R.; Jeevaratnam, K. Inhibiting bacterial colonization on catheters: Antibacterial and antibiofilm activities of bacteriocins from Lactobacillus plantarum SJ33. J. Glob. Antimicrob. Resist. 2019, 19, 85–92. [Google Scholar] [CrossRef]
  48. Botthoulath, V.; Upaichit, A.; Thumarat, U. Identification and in vitro assessment of potential probiotic characteristics and antibacterial effects of Lactobacillus plantarum subsp. plantarum SKI19, a bacteriocinogenic strain isolated from Thai fermented pork sausage. J. Food Sci. Technol. 2018, 55, 2774–2785. [Google Scholar] [CrossRef]
  49. Ahire, J.J.; Jakkamsetty, C.; Kashikar, M.S.; Lakshmi, S.G.; Madempudi, R.S. In Vitro Evaluation of Probiotic Properties of Lactobacillus plantarum UBLP40 Isolated from Traditional Indigenous Fermented Food. Probiotics Antimicrob. Proteins 2021, 13, 1413–1424. [Google Scholar] [CrossRef]
  50. Ren, D.; Li, C.; Qin, Y.; Yin, R.; Li, X.; Tian, M.; Du, S.; Guo, H.; Liu, C.; Zhu, N.; et al. Inhibition of Staphylococcus aureus adherence to Caco-2 cells by lactobacilli and cell surface properties that influence attachment. Anaerobe 2012, 18, 508–515. [Google Scholar] [CrossRef]
  51. Pasteris, S.E.; Pingitore, E.V.; Babot, G.R.; Otero, M.C.; Bühler, M.I.; Nader-Macías, M.E. Characterization of the beneficial properties of lactobacilli isolated from bullfrog (Rana catesbeiana) hatchery. Antonie Van Leeuwenhoek 2009, 95, 373–385. [Google Scholar] [CrossRef] [PubMed]
  52. Lagrafeuille, R.; Miquel, S.; Balestrino, D.; Vareille-Delarbre, M.; Chain, F.; Langella, P.; Forestier, C. Opposing effect of Lactobacillus on in vitro Klebsiella pneumoniae in biofilm and in an in vivo intestinal colonisation model. Benef. Microbes 2018, 9, 87–100. [Google Scholar] [CrossRef] [PubMed]
  53. Sürmeli, M.; Maçin, S.; Akyön, Y.; Kayikçioğlu, A.U. The protective effect of Lactobacillus plantarum against meticillin-resistant Staphylococcus aureus infections: An experimental animal model. J. Wound Care 2019, 28, s29–s34. [Google Scholar] [CrossRef] [PubMed]
  54. Ong, J.S.; Taylor, T.D.; Yong, C.C.; Khoo, B.Y.; Sasidharan, S.; Choi, S.B.; Ohno, H.; Liong, M.T. Lactobacillus plantarum USM8613 Aids in Wound Healing and Suppresses Staphylococcus aureus Infection at Wound Sites. Probiotics Antimicrob. Proteins 2020, 12, 125–137. [Google Scholar] [CrossRef]
  55. Gan, B.S.; Kim, J.; Reid, G.; Cadieux, P.; Howard, J.C. Lactobacillus fermentum RC-14 Inhibits Staphylococcus aureus Infection of Surgical Implants in Rats. J. Infect. Dis. 2002, 185, 1369–1372. [Google Scholar] [CrossRef]
  56. Fuochi, V.; Volti, G.; Furneri, P. Probiotic Properties of Lactobacillus fermentum Strains Isolated from Human Oral Samples and Description of their Antibacterial Activity. Curr. Pharm. Biotechnol. 2017, 18, 138–149. [Google Scholar] [CrossRef]
  57. Shokri, D.; Khorasgani, M.R.; Mohkam, M.; Fatemi, S.M.; Ghasemi, Y.; Taheri-Kafrani, A. The Inhibition Effect of Lactobacilli Against Growth and Biofilm Formation of Pseudomonas aeruginosa. Probiotics Antimicrob. Proteins 2018, 10, 34–42. [Google Scholar] [CrossRef]
  58. Alexandre, Y.; le Berre, R.; Barbier, G.; le Blay, G. Screening of Lactobacillus spp. for the prevention of Pseudomonas aeruginosa pulmonary infections. BMC Microbiol. 2014, 14, 107. [Google Scholar]
  59. Varma, P.; Nisha, N.; Dinesh, K.R.; Kumar, A.V.; Biswas, R. Anti-Infective Properties of Lactobacillus fermentum against Staphylococcus aureus and Pseudomonas aeruginosa. Microb. Physiol. 2011, 20, 137–143. [Google Scholar] [CrossRef]
  60. Chatterjee, M.; Pushkaran, A.C.; Vasudevan, A.K.; Menon, K.; Biswas, R.; Mohan, C.G. Understanding the adhesion mechanism of a mucin binding domain from Lactobacillus fermentum and its role in enteropathogen exclusion. Int. J. Biol. Macromol. 2018, 110, 598–607. [Google Scholar] [CrossRef]
  61. Rybalchenko, O.V.; Bondarenko, V.M.; Orlova, O.G.; Markov, A.G.; Amasheh, S. Inhibitory effects of Lactobacillus fermentum on microbial growth and biofilm formation. Arch. Microbiol. 2015, 197, 1027–1032. [Google Scholar] [CrossRef] [PubMed]
  62. Sriphannam, W.; Lumyong, S.; Niumsap, P.; Ashida, H.; Yamamoto, K.; Khanongnuch, C. A selected probiotic strain of Lactobacillus fermentum CM33 isolated from breast-fed infants as a potential source of β-galactosidase for prebiotic oligosaccharide synthesis. J. Microbiol. 2012, 50, 119–126. [Google Scholar] [CrossRef] [PubMed]
  63. Chandla, S.; Harjai, K.; Shukla, G. Synergistic Effect of Biogenics Derived from Potential Probiotics Together with Zingerone Against Biofilm Formation by Pseudomonas aeruginosa PAO1. Probiotics Antimicrob. Proteins 2021, 13, 1481–1497. [Google Scholar] [CrossRef] [PubMed]
  64. Kaewnopparat, S.; Dangmanee, N.; Kaewnopparat, N.; Srichana, T.; Chulasiri, M.; Settharaksa, S. In vitro probiotic properties of Lactobacillus fermentum SK5 isolated from vagina of a healthy woman. Anaerobe 2013, 22, 6–13. [Google Scholar] [CrossRef]
  65. Scillato, M.; Spitale, A.; Mongelli, G.; Privitera, G.F.; Mangano, K.; Cianci, A.; Stefani, S.; Santagati, M. Antimicrobial properties of Lactobacillus cell-free supernatants against multidrug-resistant urogenital pathogens. Microbiologyopen 2021, 10, e1173. [Google Scholar]
  66. Spacova, I.; O’neill, C.; Lebeer, S. Lacticaseibacillus rhamnosus GG inhibits infection of human keratinocytes by Staphylococcus aureus through mechanisms involving cell surface molecules and pH reduction. Benef. Microbes 2020, 11, 703–715. [Google Scholar] [CrossRef]
  67. Affhan, S.; Dachang, W.; Xin, Y.; Shang, D. Lactic acid bacteria protect human intestinal epithelial cells from Staphylococcus aureus and Pseudomonas aeruginosa infections. Genet. Mol. Res. 2015, 14, 17044–17058. [Google Scholar] [CrossRef]
  68. Sambanthamoorthy, K.; Feng, X.; Patel, R.; Patel, S.; Paranavitana, C. Antimicrobial and antibiofilm potential of biosurfactants isolated from lactobacilli against multi-drug-resistant pathogens. BMC Microbiol. 2014, 14, 197. [Google Scholar] [CrossRef]
  69. Kumar, A.; Kumar, D. Characterization of Lactobacillus isolated from dairy samples for probiotic properties. Anaerobe 2015, 33, 117–123. [Google Scholar] [CrossRef]
  70. Song, H.; Lou, N.; Liu, J.; Xiang, H.; Shang, D. Label-free quantitative proteomic analysis of the inhibition effect of Lactobacillus rhamnosus GG on Escherichia coli biofilm formation in co-culture. Proteome Sci. 2021, 19, 4. [Google Scholar] [CrossRef]
  71. Petrova, M.I.; Imholz, N.C.E.; Verhoeven, T.L.A.; Balzarini, J.; Van Damme, E.J.M.; Schols, D.; Vanderleyden, J.; Lebeer, S. Lectin-Like Molecules of Lactobacillus rhamnosus GG Inhibit Pathogenic Escherichia coli and Salmonella Biofilm Formation. PLoS ONE 2016, 11, e0161337. [Google Scholar] [CrossRef] [PubMed]
  72. Pascual, L.M.; Daniele, M.B.; Ruiz, F.; Giordano, W.; Pájaro, C.; Barberis, L. Lactobacillus rhamnosus L60, a potential probiotic isolated from the human vagina. J. Gen. Appl. Microbiol. 2008, 54, 141–148. [Google Scholar] [CrossRef] [PubMed]
  73. Gutiérrez, S.; Martínez-Blanco, H.; Rodríguez-Aparicio, L.B.; Ferrero, M.A. Effect of fermented broth from lactic acid bacteria on pathogenic bacteria proliferation. J. Dairy Sci. 2016, 99, 2654–2665. [Google Scholar] [CrossRef] [PubMed]
  74. Ghane, M.; Babaeekhou, L.; Ketabi, S.S. Antibiofilm Activity of Kefir Probiotic Lactobacilli Against Uropathogenic Escherichia coli (UPEC). Avicenna J. Med. Biotechnol. 2020, 12, 221–229. [Google Scholar]
  75. Liu, G.; Pang, B.; Li, N.; Jin, H.; Li, J.; Wu, W.; Ai, C.; Jiang, C.; Shi, J. Therapeutic effect of Lactobacillus rhamnosus SHA113 on intestinal infection by multi-drug-resistant Staphylococcus aureus and its underlying mechanisms. Food Funct. 2020, 11, 6226–6239. [Google Scholar] [CrossRef]
  76. Zhou, B.; Zhang, D. Antibacterial effects of bacteriocins isolated from Lactobacillus rhamnosus (ATCC 53103) in a rabbit model of knee implant infection. Exp. Ther. Med. 2018, 15, 2985–2989. [Google Scholar] [CrossRef]
  77. Muñoz-Quezada, S.; Bermudez-Brito, M.; Chenoll, E.; Genovés, S.; Gomez-Llorente, C.; Plaza-Diaz, J.; Matencio, E.; José Bernal, M.; Romero, F.; Ramón, D.; et al. Competitive inhibition of three novel bacteria isolated from faeces of breast milk-fed infants against selected enteropathogens. Br. J. Nutr. 2013, 109, S63–S69. [Google Scholar] [CrossRef]
  78. Rahne, M.; Basic, A.; Almståhl, A. Explorative study on Lactobacillus species and their acid-producing capacity and anti-microbial activity in head and neck cancer patients. Clin. Exp. Dent. Res. 2021, 7, 924–933. [Google Scholar] [CrossRef]
  79. El-Mokhtar, M.A.; Hassanein, K.M.; Ahmed, A.S.; Gad, G.F.; Amin, M.M.; Hassanein, O.F. Antagonistic Activities of Cell-Free Supernatants of Lactobacilli Against Extended-Spectrum β-Lactamase Producing Klebsiella pneumoniae and Pseudomonas aeruginosa. Infect. Drug Resist. 2020, 13, 543–552. [Google Scholar] [CrossRef]
  80. Kim, Y.; Kim, S.-H.; Whang, K.-Y.; Kim, Y.-J.; Oh, S. Inhibition of Escherichia coli O157:H7 attachment by interactions between lactic acid bacteria and intestinal epithelial cells. J. Microbiol. Biotechnol. 2008, 18, 1278–1285. [Google Scholar]
  81. Sadowska, B.; Walencka, E.; Wieckowska-Szakiel, M.; Różalska, B. Bacteria competing with the adhesion and biofilm formation by Staphylococcus aureus. Folia Microbiol. 2010, 55, 497–501. [Google Scholar] [CrossRef] [PubMed]
  82. Walencka, E.; Różalska, S.; Sadowska, B. The influence of Lactobacillus acidophilus-derived surfactants on staphylococcal adhesion and biofilm formation. Folia Microbiol. 2008, 53, 61–66. [Google Scholar] [CrossRef] [PubMed]
  83. Fourniat, J.; Colomban, C.; Linxe, C.; Karam, D. Heat-killed Lactobacillus acidophilus inhibits adhesion of Escherichia coli B41 to HeLa cells. Ann. Rech. Vet. 1992, 23, 361–370. [Google Scholar] [PubMed]
  84. Meng, J.; Gao, S.-M.; Zhang, Q.-X.; Lu, R.-R. Murein hydrolase activity of surface layer proteins from Lactobacillus acidophilus against Escherichia coli. Int. J. Biol. Macromol. 2015, 79, 527–532. [Google Scholar] [CrossRef] [PubMed]
  85. Velraeds, M.M.C.; Van De Belt-Gritter, B.; Van Der Mei, H.C.; Reid, G.; Busscher, H.J. Interference in Initial Adhesion of Uropathogenic Bacteria and Yeasts to Silicone Rubber by A Lactobacillus acidophilus Biosurfactant. J. Med. Microbiol. 1998, 47, 1081–1085. [Google Scholar] [CrossRef]
  86. Abo-Amer, A. Molecular characterization of antimicrobial compound produced by Lactobacillus acidophilus AA11. Acta Microbiol. Immunol. Hung. 2007, 54, 107–119. [Google Scholar] [CrossRef]
  87. Gaspar, C.; Donders, G.G.; Palmeira-De-Oliveira, R.; Queiroz, J.A.; Tomaz, C.; Martinez-De-Oliveira, J. Bacteriocin production of the probiotic Lactobacillus acidophilus KS400. AMB Express 2018, 8, 153. [Google Scholar] [CrossRef]
  88. Koohestani, M.; Moradi, M.; Tajik, H.; Badali, A. Effects of cell-free supernatant of Lactobacillus acidophilus LA5 and Lactobacillus casei 431 against planktonic form and biofilm of Staphylococcus aureus. Vet. Res. Forum 2018, 9, 301–306. [Google Scholar]
  89. Coconnier, M.H.; Bernet, M.F.; Chauvière, G.; Servin, A.L. Adhering heat-killed human Lactobacillus acidophilus, strain LB, inhibits the process of pathogenicity of diarrhoeagenic bacteria in cultured human intestinal cells. J. Diarrhoeal Dis. Res. 1993, 11, 235–242. [Google Scholar]
  90. Sharma, K.; Mahajan, R.; Attri, S.; Goel, G. Selection of indigenous Lactobacillus paracasei CD4 and Lactobacillus gastricus BTM 7 as probiotic: Assessment of traits combined with principal component analysis. J. Appl. Microbiol. 2017, 122, 1310–1320. [Google Scholar] [CrossRef]
  91. Gudiña, E.J.; Rocha, V.; Teixeira, J.A.; Rodrigues, L.R. Antimicrobial and antiadhesive properties of a biosurfactant isolated from Lactobacillus paracasei Ssp. paracasei A20. Lett. Appl. Microbiol. 2010, 50, 419–424. [Google Scholar] [CrossRef] [PubMed]
  92. Gudiña, E.J.; Teixeira, J.A.; Rodrigues, L.R. Isolation and functional characterization of a biosurfactant produced by Lactobacillus paracasei. Colloids Surf. B Biointerfaces 2010, 76, 298–304. [Google Scholar] [CrossRef] [PubMed]
  93. Ocaña, V.S.; de Ruiz Holgado, A.A.; Nader-Macías, M.E. Growth inhibition of Staphylococcus aureus by H2O2-producing Lactobacillus paracasei subsp. paracasei isolated from the human vagina. FEMS Immunol. Med. Microbiol. 1999, 23, 87–92. [Google Scholar] [CrossRef] [PubMed]
  94. Liang, T.-W.; Wu, Y.-Y.; Huang, T.-Y.; Wang, C.-Y.; Yen, Y.-H.; Liu, C.-P.; Chen, Y.-C.; Wang, S.-L. Conversion of squid pen by a novel strain Lactobacillus paracasei subsp. paracasei TKU010, and its application in antimicrobial and antioxidants activity. J. Gen. Appl. Microbiol. 2010, 56, 481–489. [Google Scholar] [CrossRef] [PubMed]
  95. Xu, X.; Peng, Q.; Zhang, Y.; Tian, D.; Zhang, P.; Huang, Y.; Ma, L.; Dia, V.P.; Qiao, Y.; Shi, B. Antibacterial potential of a novel Lactobacillus casei strain isolated from Chinese northeast sauerkraut and the antibiofilm activity of its exopolysaccharides. Food Funct. 2020, 11, 4697–4706. [Google Scholar] [CrossRef] [PubMed]
  96. Peng, M.; Tabashsum, Z.; Patel, P.; Bernhardt, C.; Biswas, D. Linoleic Acids Overproducing Lactobacillus casei Limits Growth, Survival, and Virulence of Salmonella Typhimurium and Enterohaemorrhagic Escherichia coli. Front. Microbiol. 2018, 9, 2663. [Google Scholar] [CrossRef] [PubMed]
  97. Zavišić, G.; Ristic, S.; Petrièević, S.; Jovanović, J.N.; Raduloviæ, Ž.; Petković, B.J.; Strahinic, I.; Piperski, V.; Zavišiæ, G.; Ristiæ, S.; et al. Characterisation and preliminary lipid-lowering evaluation of Lactobacillus isolated from a traditional Serbian dairy product. Benef. Microbes 2015, 6, 119–128. [Google Scholar] [CrossRef] [PubMed]
  98. Da Silva, J.A.; De Siqueira-Júnior, J.P. Nature of the antimicrobial activity of Lactobacillus casei, Bifidobacterium bifidum and Bifidobacterium animalis against foodborne pathogenic and spoilage microorganisms. Nat. Prod. Res. 2015, 29, 2133–2136. [Google Scholar] [CrossRef]
  99. Merghni, A.; Dallel, I.; Noumi, E.; Kadmi, Y.; Hentati, H.; Tobji, S.; Ben Amor, A.; Mastouri, M. Antioxidant and antiproliferative potential of biosurfactants isolated from Lactobacillus casei and their anti-biofilm effect in oral Staphylococcus aureus strains. Microb. Pathog. 2017, 104, 84–89. [Google Scholar] [CrossRef]
  100. Souza, R.F.S.; Jardin, J.; Cauty, C.; Rault, L.; Bouchard, D.S.; Bermúdez-Humarán, L.G.; Langella, P.; Monedero, V.; Seyffert, N.; Azevedo, V.; et al. Contribution of sortase SrtA2 to Lactobacillus casei BL23 inhibition of Staphylococcus aureus internalization into bovine mammary epithelial cells. PLoS ONE 2017, 12, e0174060. [Google Scholar] [CrossRef]
  101. Meng, J.; Wang, Y.-Y.; Hao, Y.-P. Protective function of surface layer protein from Lactobacillus casei fb05 against intestinal pathogens in vitro. Biochem. Biophys. Res. Commun. 2021, 546, 15–20. [Google Scholar] [CrossRef] [PubMed]
  102. Gómez, N.C.; Ramiro, J.M.P.; Quecan, B.X.V.; Franco, B.D.G.D.M. Use of Potential Probiotic Lactic Acid Bacteria (LAB) Biofilms for the Control of Listeria monocytogenes, Salmonella typhimurium, and Escherichia coli O157:H7 Biofilms Formation. Front. Microbiol. 2016, 7, 863. [Google Scholar] [CrossRef] [PubMed]
  103. Singh, T.P.; Kaur, G.; Kapila, S.; Malik, R.K. Antagonistic Activity of Lactobacillus reuteri Strains on the Adhesion Characteristics of Selected Pathogens. Front. Microbiol. 2017, 8, 486. [Google Scholar] [CrossRef] [PubMed]
  104. Mulla, M.; Mulla, M.; Hegde, S.; Koshy, A.V. In vitro assessment of the effect of probiotic Lactobacillus reuteri on peri-implantitis microflora. BMC Oral Health 2021, 21, 408. [Google Scholar] [CrossRef] [PubMed]
  105. Laughton, J.M.; Devillard, E.; Heinrichs, D.E.; Reid, G.; McCormick, J.K. Inhibition of expression of a staphylococcal superantigen-like protein by a soluble factor from Lactobacillus reuteri. Microbiology 2006, 152, 1155–1167. [Google Scholar] [CrossRef]
  106. Rajoka, M.S.R.; Mehwish, H.M.; Hayat, H.F.; Hussain, N.; Sarwar, S.; Aslam, H.; Nadeem, A.; Shi, J. Characterization, the Antioxidant and Antimicrobial Activity of Exopolysaccharide Isolated from Poultry Origin Lactobacilli. Probiotics Antimicrob. Proteins 2019, 11, 1132–1142. [Google Scholar] [CrossRef]
  107. Al-Dhabi, N.A.; Arasu, M.V.; Vijayaraghavan, P.; Esmail, G.A.; Duraipandiyan, V.; Kim, Y.O.; Kim, H.; Kim, H.-J. Probiotic and Antioxidant Potential of Lactobacillus reuteri LR12 and Lactobacillus lactis LL10 Isolated from Pineapple Puree and Quality Analysis of Pineapple-Flavored Goat Milk Yoghurt during Storage. Microorganisms 2020, 8, 1461. [Google Scholar] [CrossRef]
  108. Hojjati, M.; Behabahani, B.A.; Falah, F. Aggregation, adherence, anti-adhesion and antagonistic activity properties relating to surface charge of probiotic Lactobacillus brevis gp104 against Staphylococcus aureus. Microb. Pathog. 2020, 147, 104420. [Google Scholar] [CrossRef]
  109. Son, S.-H.; Jeon, H.-L.; Yang, S.-J.; Lee, N.-K.; Paik, H.-D. In vitro characterization of Lactobacillus brevis KU15006, an isolate from kimchi, reveals anti-adhesion activity against foodborne pathogens and antidiabetic properties. Microb. Pathog. 2017, 112, 135–141. [Google Scholar] [CrossRef]
  110. Jang, H.J.; Lee, N.-K.; Paik, H.-D. Probiotic characterization of Lactobacillus brevis KU15153 showing antimicrobial and antioxidant effect isolated from kimchi. Food Sci. Biotechnol. 2019, 28, 1521–1528. [Google Scholar] [CrossRef]
  111. Kang, M.-S.; Lim, H.-S.; Oh, J.-S.; Lim, Y.-J.; Wuertz-Kozak, K.; Harro, J.M.; Shirtliff, M.E.; Achermann, Y. Antimicrobial activity of Lactobacillus salivarius and Lactobacillus fermentum against Staphylococcus aureus. Pathog. Dis. 2017, 75, 2. [Google Scholar] [CrossRef] [PubMed]
  112. Arihara, K.; Ogihara, S.; Mukai, T.; Itoh, M.; Kondo, Y. Salivacin 140, a novel bacteriocin from Lactobacillus salivarius subsp. salicinius T140 active against pathogenic bacteria. Lett. Appl. Microbiol. 1996, 22, 420–424. [Google Scholar] [CrossRef] [PubMed]
  113. Mahdi, L.H.; Jabbar, H.S.; Auda, I.G. Antibacterial immunomodulatory and antibiofilm triple effect of Salivaricin LHM against Pseudomonas aeruginosa urinary tract infection model. Int. J. Biol. Macromol. 2019, 134, 1132–1144. [Google Scholar] [CrossRef]
  114. Jiang, X.; Yan, X.; Gu, S.; Yang, Y.; Zhao, L.; He, X.; Chen, H.; Ge, J.; Liu, D. Biosurfactants of Lactobacillus helveticus for biodiversity inhibit the biofilm formation of Staphylococcus aureus and cell invasion. Futur. Microbiol. 2019, 14, 1133–1146. [Google Scholar] [CrossRef] [PubMed]
  115. Johnson-Henry, K.C.; Hagen, K.E.; Gordonpour, M.; Tompkins, T.A.; Sherman, P.M. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell. Microbiol. 2007, 9, 356–367. [Google Scholar] [CrossRef]
  116. Yang, J.; Wang, J.; Yang, K.; Liu, M.; Qi, Y.; Zhang, T.; Fan, M.; Wei, X. Antibacterial activity of selenium-enriched lactic acid bacteria against common food-borne pathogens in vitro. J. Dairy Sci. 2018, 101, 1930–1942. [Google Scholar] [CrossRef] [PubMed]
  117. Batdorj, B.; Trinetta, V.; Dalgalarrondo, M.; Prévost, H.; Dousset, X.; Ivanova, I.; Haertlé, T.; Chobert, J.M. Isolation, taxonomic identification and hydrogen peroxide production by Lactobacillus delbrueckii subsp. lactis T31, isolated from Mongolian yoghurt: Inhibitory activity on food-borne pathogens. J. Appl. Microbiol. 2007, 103, 584–593. [Google Scholar] [CrossRef] [PubMed]
  118. Kaur, S.; Sharma, P. Protease-Sensitive Inhibitory Activity of Cell-free Supernatant of Lactobacillus crispatus 156 Synergizes with Ciprofloxacin, Moxifloxacin and Streptomycin against Pseudomonas aeruginosa: An In Vitro Study. Probiotics Antimicrob. Proteins 2015, 7, 172–180. [Google Scholar] [CrossRef]
  119. Atassi, F.; Ahn, D.L.P.V.; Moal, V.L.-L. Diverse Expression of Antimicrobial Activities Against Bacterial Vaginosis and Urinary Tract Infection Pathogens by Cervicovaginal Microbiota Strains of Lactobacillus gasseri and Lactobacillus crispatus. Front. Microbiol. 2019, 10, 2900. [Google Scholar] [CrossRef]
  120. Ouali, F.A.; Al Kassaa, I.; Cudennec, B.; Abdallah, M.; Bendali, F.; Sadoun, D.; Chihib, N.-E.; Drider, D. Identification of lactobacilli with inhibitory effect on biofilm formation by pathogenic bacteria on stainless steel surfaces. Int. J. Food Microbiol. 2014, 191, 116–124. [Google Scholar] [CrossRef]
  121. Giordani, B.; Costantini, P.E.; Fedi, S.; Cappelletti, M.; Abruzzo, A.; Parolin, C.; Foschi, C.; Frisco, G.; Calonghi, N.; Cerchiara, T.; et al. Liposomes containing biosurfactants isolated from Lactobacillus gasseri exert antibiofilm activity against methicillin resistant Staphylococcus aureus strains. Eur. J. Pharm. Biopharm. 2019, 139, 246–252. [Google Scholar] [CrossRef] [PubMed]
  122. Shi, S.; Cheng, B.; Gu, B.; Sheng, T.; Tu, J.; Shao, Y.; Qi, K.; Zhou, D. Evaluation of the probiotic and functional potential of Lactobacillus agilis 32 isolated from pig manure. Lett. Appl. Microbiol. 2021, 73, 9–19. [Google Scholar] [CrossRef]
  123. Berríos, P.; Fuentes, J.; Salas, D.; Carreño, A.; Aldea, P.; Fernández, F.; Trombert, A. Inhibitory effect of biofilm-forming Lactobacillus kunkeei strains against virulent Pseudomonas aeruginosa in vitro and in honeycomb moth (Galleria mellonella) infection model. Benef. Microbes 2018, 9, 257–268. [Google Scholar] [CrossRef] [PubMed]
  124. Perelmuter, K.; Fraga, M.; Zunino, P. In vitro activity of potential probiotic Lactobacillus murinus isolated from the dog. J. Appl. Microbiol. 2008, 104, 1718–1725. [Google Scholar] [CrossRef]
  125. Wu, S.; Hou, W.; Suo, X.; Guo, X.; Li, H. Bacillus subtilis extracellular polymeric substances conditioning layers inhibit Escherichia coli adhesion to silicon surfaces: A potential candidate for interfacial antifouling additives. Biointerphases 2021, 16, 011003. [Google Scholar] [CrossRef] [PubMed]
  126. Algburi, A.; Al-Hasani, H.M.; Ismael, T.K.; Abdelhameed, A.; Weeks, R.; Ermakov, A.M.; Chikindas, M.L. Antimicrobial Activity of Bacillus subtilis KATMIRA1933 and Bacillus amyloliquefaciens B-1895 against Staphylococcus aureus Biofilms Isolated from Wound Infection. Probiotics Antimicrob. Proteins 2021, 13, 125–134. [Google Scholar] [CrossRef]
  127. Kalpana, B.J.; Aarthy, S.; Pandian, S.K. Antibiofilm Activity of α-Amylase from Bacillus subtilis S8-18 Against Biofilm Forming Human Bacterial Pathogens. Appl. Biochem. Biotechnol. 2012, 167, 1778–1794. [Google Scholar] [CrossRef]
  128. Taggar, R.; Singh, S.; Bhalla, V.; Bhattacharyya, M.S.; Sahoo, D.K. Deciphering the Antibacterial Role of Peptide from Bacillus subtilis subsp. spizizenii Ba49 against Staphylococcus aureus. Front. Microbiol. 2021, 12, 708712. [Google Scholar] [CrossRef]
  129. Freitas, F.D.S.; Lage, T.C.D.A.; Ayupe, B.A.L.; Siqueira, T.D.P.; de Barros, M.; Tótola, M.R. Bacillus subtilis TR47II as a source of bioactive lipopeptides against Gram-negative pathogens causing nosocomial infections. 3 Biotech 2020, 10, 474. [Google Scholar] [CrossRef]
  130. Afroj, S.; Brannen, A.D.; Nasrin, S.; Al Mouslem, A.; Hathcock, T.; Maxwell, H.; Rasmussen-Ivey, C.R.; Sandage, M.J.; Davis, E.W.; Panizzi, P.; et al. Bacillus velezensis AP183 Inhibits Staphylococcus aureus Biofilm Formation and Proliferation in Murine and Bovine Disease Models. Front. Microbiol. 2021, 12, 746410. [Google Scholar] [CrossRef]
  131. Baharudin, M.M.A.-A.; Ngalimat, M.S.; Shariff, F.M.; Yusof, Z.N.B.; Karim, M.; Baharum, S.N.; Sabri, S. Antimicrobial activities of Bacillus velezensis strains isolated from stingless bee products against methicillin-resistant Staphylococcus aureus. PLoS ONE 2021, 16, e0251514. [Google Scholar] [CrossRef]
  132. Basit, M.; Rasool, M.H.; Naqvi, S.A.R.; Waseem, M.; Aslam, B. Biosurfactants production potential of native strains of Bacillus cereus and their antimicrobial, cytotoxic and antioxidant activities. Pak. J. Pharm. Sci. 2018, 31, 251–256. [Google Scholar] [PubMed]
  133. Saggese, A.; Culurciello, R.; Casillo, A.; Corsaro, M.M.; Ricca, E.; Baccigalupi, L. A Marine Isolate of Bacillus pumilus Secretes a Pumilacidin Active against Staphylococcus aureus. Mar. Drugs 2018, 16, 180. [Google Scholar] [CrossRef] [PubMed]
  134. Shivangi, S.; Devi, P.B.; Ragul, K.; Shetty, P.H. Probiotic Potential of Bacillus Strains Isolated from an Acidic Fermented Food Idli. Probiotics Antimicrob. Proteins 2020, 12, 1502–1513. [Google Scholar] [CrossRef] [PubMed]
  135. Cisneros, L.; Cattelan, N.; Villalba, M.; Rodriguez, C.; Serra, D.; Yantorno, O.; Fadda, S. Lactic acid bacteria biofilms and their ability to mitigate Escherichia coli O157:H7 surface colonization. Lett. Appl. Microbiol. 2021, 73, 247–256. [Google Scholar] [CrossRef]
  136. Nigatu, A.; Gashe, B.A. Survival and growth of selected pathogens in fermented kocho (Ensete ventricosum). East Afr. Med. J. 1994, 71, 514–518. [Google Scholar]
  137. Alvarado, C.; Almendárez, B.E.G.; Martin, S.E.; Regalado, C. Food-associated lactic acid bacteria with antimicrobial potential from traditional Mexican foods. Rev. Latinoam. Microbiol. 2006, 48, 260–268. [Google Scholar]
  138. Badwaik, L.S.; Borah, P.K.; Deka, S.C. Production and Purification of Anti-Bacterial Biometabolite from Wild-Type Lactobacillus, Isolated from Fermented Bamboo Shoot: Future Suggestions and a Proposed System for Secondary Metabolite Onsite Recovery During Continuous Fermentation. Appl. Biochem. Biotechnol. 2015, 175, 1915–1925. [Google Scholar] [CrossRef]
  139. Graves, R.R.; Frazier, W.C. Food Microorganisms Influencing the Growth of Staphylococcus aureus. Appl. Microbiol. 1963, 11, 513–516. [Google Scholar] [CrossRef]
  140. Dembélé, T.; Obdrálek, V.; Votava, M. Inhibition of bacterial pathogens by lactobacilli. Zent. Bakteriol. 1998, 288, 395–401. [Google Scholar] [CrossRef]
  141. Millette, M.; Dupont, C.; Archambault, D.; Lacroix, M. Partial characterization of bacteriocins produced by human Lactococcus lactis and Pediococccus acidilactici isolates. J. Appl. Microbiol. 2007, 102, 274–282. [Google Scholar] [CrossRef] [PubMed]
  142. Zhang, W.; Wang, H.; Liu, J.; Zhao, Y.; Gao, K.; Zhang, J. Adhesive ability means inhibition activities for lactobacillus against pathogens and S-layer protein plays an important role in adhesion. Anaerobe 2013, 22, 97–103. [Google Scholar] [CrossRef] [PubMed]
  143. Chan, R.C.; Reid, G.; Irvin, R.T.; Bruce, A.W.; Costerton, J.W. Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments. Infect. Immun. 1985, 47, 84–89. [Google Scholar] [CrossRef] [PubMed]
  144. Stone, W.; Tolmay, J.; Tucker, K.; Wolfaardt, G.M. Disinfectant, Soap or Probiotic Cleaning? Surface Microbiome Diversity and Biofilm Competitive Exclusion. Microorganisms 2020, 8, 1726. [Google Scholar] [CrossRef] [PubMed]
  145. Silvaderuiz, C.; Lopezdebocanera, M.E.; Naderdemacias, M.E.; Pescederuizholgado, A.A. Effect of Lactobacilli and Antibiotics on E. coli Urinary Infections in Mice. Biol. Pharm. Bull. 1996, 19, 88–93. [Google Scholar] [CrossRef] [PubMed]
  146. Kermanshahi, R.K.; Feizabadi, M.M. The Inhibitory Effects of Lactobacillus Supernatants and Their Metabolites on the Growth and Biofilm Formation of Klebsiella pneumoniae. Infect. Disord.—Drug Targets 2021, 20, 902–912. [Google Scholar] [CrossRef]
  147. Turková, K.; Mavrič, A.; Narat, M.; Rittich, B.; Španová, A.; Rogelj, I.; Matijašić, B.B. Evaluation of Lactobacillus strains for selected probiotic properties. Folia Microbiol. 2013, 58, 261–267. [Google Scholar] [CrossRef]
  148. Lee, Y.-K.; Puong, K.-Y.; Ouwehand, A.; Salminen, S. Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. J. Med. Microbiol. 2003, 52, 925–930. [Google Scholar] [CrossRef]
  149. Lu, Y.; Yan, H.; Li, X.; Gu, Y.; Wang, X.; Yi, Y.; Shan, Y.; Liu, B.; Zhou, Y.; Lü, X. Physicochemical properties and mode of action of a novel bacteriocin BM1122 with broad antibacterial spectrum produced by Lactobacillus crustorum MN047. J. Food Sci. 2020, 85, 1523–1535. [Google Scholar] [CrossRef]
  150. Haines, W.C.; Harmon, L.G. Effect of Selected Lactic Acid Bacteria on Growth of Staphylococcus aureus and Production of Enterotoxin. Appl. Microbiol. 1973, 25, 436–441. [Google Scholar] [CrossRef]
  151. Turner, M.S.; Waldherr, F.; Loessner, M.J.; Giffard, P.M. Antimicrobial activity of lysostaphin and a Listeria monocytogenes bacteriophage endolysin produced and secreted by lactic acid bacteria. Syst. Appl. Microbiol. 2007, 30, 58–67. [Google Scholar] [CrossRef] [PubMed]
  152. McMillan, A.; Dell, M.; Zellar, M.P.; Cribby, S.; Martz, S.; Hong, E.; Fu, J.; Abbas, A.; Dang, T.; Miller, W.; et al. Disruption of urogenital biofilms by lactobacilli. Colloids Surf. B Biointerfaces 2011, 86, 58–64. [Google Scholar] [CrossRef]
  153. Chappell, T.C.; Nair, N.U. Engineered lactobacilli display anti-biofilm and growth suppressing activities against Pseudomonas aeruginosa. Npj Biofilms Microbiomes 2020, 6, 48. [Google Scholar] [CrossRef] [PubMed]
  154. Qiao, Z.; Chen, J.; Zhou, Q.; Wang, X.; Shan, Y.; Yi, Y.; Liu, B.; Zhou, Y.; Lü, X. Purification, characterization, and mode of action of a novel bacteriocin BM173 from Lactobacillus crustorum MN047 and its effect on biofilm formation of Escherichia coli and Staphylococcus aureus. J. Dairy Sci. 2021, 104, 1474–1483. [Google Scholar] [CrossRef] [PubMed]
  155. Kiymaci, M.E.; Altanlar, N.; Gumustas, M.; Ozkan, S.A.; Akin, A. Quorum sensing signals and related virulence inhibition of Pseudomonas aeruginosa by a potential probiotic strain’s organic acid. Microb. Pathog. 2018, 121, 190–197. [Google Scholar] [CrossRef] [PubMed]
  156. Ramos, A.N.; Sesto Cabral, M.E.; Arena, M.E.; Arrighi, C.F.; Arroyo Aguilar, A.A.; Valdéz, J.C. Compounds from Lactobacillus plantarum culture supernatants with potential pro-healing and anti-pathogenic properties in skin chronic wounds. Pharm. Biol. 2015, 53, 350–358. [Google Scholar] [CrossRef]
  157. Shaaban, M.; El-Rahman, O.A.A.; Al-Qaidi, B.; Ashour, H.M. Antimicrobial and Antibiofilm Activities of Probiotic Lactobacilli on Antibiotic-Resistant Proteus mirabilis. Microorganisms 2020, 8, 960. [Google Scholar] [CrossRef]
  158. Strus, M.; Malinowska, M.; Heczko, P.B. In vitro antagonistic effect of Lactobacillus on organisms associated with bacterial vaginosis. J. Reprod. Med. 2002, 47, 41–46. [Google Scholar]
  159. Nomoto, K. Prevention of infections by probiotics. J. Biosci. Bioeng. 2005, 100, 583–592. [Google Scholar] [CrossRef]
  160. Yan, F.; Polk, D.B. Probiotics and immune health. Curr. Opin. Gastroenterol. 2011, 27, 496–501. [Google Scholar] [CrossRef]
  161. Shanahan, F. Probiotics in Perspective. Gastroenterology 2010, 139, 1808–1812. [Google Scholar] [CrossRef] [PubMed]
  162. Tappenden, K.A.; Deutsch, A.S. The physiological relevance of the intestinal microbiota--contributions to human health. J. Am. Coll. Nutr. 2007, 26, 679S–683S. [Google Scholar] [CrossRef] [PubMed]
  163. Hao, Q.; Lu, Z.; Dong, B.R.; Huang, C.Q.; Wu, T. Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Syst. Rev. 2015, 21, CD006895. [Google Scholar] [CrossRef] [PubMed]
  164. Goldin, B.R.; Gorbach, S.L. Clinical Indications for Probiotics: An Overview. Clin. Infect. Dis. 2008, 46, S96–S100. [Google Scholar] [CrossRef] [PubMed]
  165. Hamilton-Miller, J. The role of probiotics in the treatment and prevention of Helicobacter pylori infection. Int. J. Antimicrob. Agents 2003, 22, 360–366. [Google Scholar] [CrossRef] [PubMed]
  166. Espitia, P.J.; Batista, R.A.; Azeredo, H.M.; Otoni, C.G. Probiotics and their potential applications in active edible films and coatings. Food Res. Int. 2016, 90, 42–52. [Google Scholar] [CrossRef]
  167. Hossain, I.; Sadekuzzaman, M.; Ha, S.-D. Probiotics as potential alternative biocontrol agents in the agriculture and food industries: A review. Food Res. Int. 2017, 100, 63–73. [Google Scholar] [CrossRef]
  168. Bennett, B. Gastroenteritis. Med. Update Psychiatr. 1998, 3, 95–98. [Google Scholar] [CrossRef]
  169. Raposo, A.; Pérez, E.; de Faria, C.T.; Ferrús, M.A.; Carrascosa, C. Food Spoilage by Pseudomonas spp.—An Overview. In Foodborne Pathogens and Antibiotic Resistance; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2017; pp. 41–71. [Google Scholar] [CrossRef]
  170. McFarland, L.V.; Evans, C.T.; Goldstein, E.J.C. Strain-Specificity and Disease-Specificity of Probiotic Efficacy: A Systematic Review and Meta-Analysis. Front. Med. 2018, 5, 124. [Google Scholar] [CrossRef]
  171. Lee, I.-C.; Tomita, S.; Kleerebezem, M.; Bron, P.A. The quest for probiotic effector molecules—Unraveling strain specificity at the molecular level. Pharmacol. Res. 2013, 69, 61–74. [Google Scholar] [CrossRef]
  172. Doron, S.; Snydman, D.R. Risk and Safety of Probiotics. Clin. Infect. Dis. 2015, 60, S129–S134. [Google Scholar] [CrossRef] [PubMed]
  173. Didari, T.; Solki, S.; Mozaffari, S.; Nikfar, S.; Abdollahi, M. A systematic review of the safety of probiotics. Expert Opin. Drug Saf. 2013, 13, 227–239. [Google Scholar] [CrossRef] [PubMed]
  174. La Maestra, S.; D’Agostini, F.; Geretto, M.; Micale, R.T. Microbial-based cleaning products as a potential risk to human health: A review. Toxicol. Lett. 2021, 353, 60–70. [Google Scholar] [CrossRef] [PubMed]
  175. Jeżewska-Frąckowiak, J.; Żebrowska, J.; Czajkowska, E.; Jasińska, J.; Pęksa, M.; Jędrzejczak, G.; Skowron, P. Identification of bacterial species in probiotic consortiums in selected commercial cleaning preparations. Acta Biochim. Pol. 2019, 66, 215–222. [Google Scholar] [CrossRef]
  176. Neidhöfer, C.; Buechler, C.; Neidhöfer, G.; Bierbaum, G.; Hannet, I.; Hoerauf, A.; Parčina, M. Global Distribution Patterns of Carbapenemase-Encoding Bacteria in a New Light: Clues on a Role for Ethnicity. Front. Cell. Infect. Microbiol. 2021, 11, 659753. [Google Scholar] [CrossRef]
  177. Neidhöfer, C.; Berens, C.; Parčina, M. An 18-year dataset on the clinical incidence and MICs to antibiotics of Achromobacter spp. (labeled biochemically or by MAL-DI-TOF MS as A. xylosoxidans), largely in patient groups other than those with CF. Antibiotics 2022, 11, 311. [Google Scholar] [CrossRef]
  178. Schuster, D.; Axtmann, K.; Holstein, N.; Felder, C.; Voigt, A.; Färber, H.; Ciorba, P.; Szekat, C.; Schallenberg, A.; Böckmann, M.; et al. Antibiotic concentrations in raw hospital wastewater surpass minimal selective and minimum inhibitory concentrations of resistant Acinetobacter baylyi strains. Environ. Microbiol. 2022, 24, 5721–5733. [Google Scholar] [CrossRef]
  179. Neidhöfer, C.; Sib, E.; Neuenhoff, M.; Schwengers, O.; Dummin, T.; Buechler, C.; Klein, N.; Balks, J.; Axtmann, K.; Schwab, K.; et al. Hospital sanitary facilities on wards with high antibiotic exposure play an important role in maintaining a reservoir of resistant pathogens, even over many years. Antimicrob. Resist. Infect. Control 2023, 12, 33. [Google Scholar] [CrossRef]
  180. Neidhöfer, C.; Sib, E.; Benhsain, A.-H.; Mutschnik-Raab, C.; Schwabe, A.; Wollkopf, A.; Wetzig, N.; Sieber, M.A.; Thiele, R.; Döhla, M.; et al. Examining Different Analysis Protocols Targeting Hospital Sanitary Facility Microbiomes. Microorganisms 2023, 11, 185. [Google Scholar] [CrossRef]
  181. Xue, L.; Li, Z.; Xue, J.; Wang, H.; Wu, T.; Liu, R.; Sui, W.; Zhang, M. Lactobacillus acidophilus LA85 ameliorates cyclophosphamide-induced immunosuppression by modulating Notch and TLR4/NF-κB signal pathways and remodeling the gut microbiota. Food Funct. 2022, 13, 8107–8118. [Google Scholar] [CrossRef]
  182. Goodman, C.; Keating, G.; Georgousopoulou, E.; Hespe, C.; Levett, K. Probiotics for the prevention of antibiotic-associated diarrhoea: A systematic review and meta-analysis. BMJ Open 2021, 11, e043054. [Google Scholar] [CrossRef] [PubMed]
  183. Singh, N.K.; Beckett, J.M.; Kalpurath, K.; Ishaq, M.; Ahmad, T.; Eri, R.D. Synbiotics as Supplemental Therapy for the Alleviation of Chemotherapy-Associated Symptoms in Patients with Solid Tumours. Nutrients 2023, 15, 1759. [Google Scholar] [CrossRef] [PubMed]
  184. Dikeocha, I.J.; Al-Kabsi, A.M.; Eid, E.E.M.; Hussin, S.; Alshawsh, M.A. Probiotics supplementation in patients with colorectal cancer: A systematic review of randomized controlled trials. Nutr. Rev. 2021, 80, 22–49. [Google Scholar] [CrossRef] [PubMed]
  185. Klassert, T.E.; Zubiria-Barrera, C.; Neubert, R.; Stock, M.; Schneegans, A.; López, M.; Driesch, D.; Zakonsky, G.; Gastmeier, P.; Slevogt, H.; et al. Comparative analysis of surface sanitization protocols on the bacterial community structures in the hospital environment. Clin. Microbiol. Infect. 2022, 28, 1105–1112. [Google Scholar] [CrossRef]
  186. D’accolti, M.; Soffritti, I.; Bini, F.; Mazziga, E.; Cason, C.; Comar, M.; Volta, A.; Bisi, M.; Fumagalli, D.; Mazzacane, S.; et al. Shaping the subway microbiome through probiotic-based sanitation during the COVID-19 emergency: A pre–post case–control study. Microbiome 2023, 11, 64. [Google Scholar] [CrossRef]
  187. Soffritti, I.; D’Accolti, M.; Cason, C.; Lanzoni, L.; Bisi, M.; Volta, A.; Campisciano, G.; Mazzacane, S.; Bini, F.; Mazziga, E.; et al. Introduction of Probiotic-Based Sanitation in the Emergency Ward of a Children’s Hospital During the COVID-19 Pandemic. Infect. Drug Resist. 2022, 15, 1399–1410. [Google Scholar] [CrossRef] [PubMed]
Antibiotics 12 00871 g001 550
Figure 1. Study flow diagram.
Figure 1. Study flow diagram.
Antibiotics 12 00871 g001
Table
Table 1. List of probiotic bacteria, and number of cases in which antibacterial properties were attributed to them against one or more of the three most frequently tested ESKAPEE pathogens.
Table 1. List of probiotic bacteria, and number of cases in which antibacterial properties were attributed to them against one or more of the three most frequently tested ESKAPEE pathogens.
S. aureusE. coliP. aeruginosa
Lactiplantibacillus plantarum231612
Lactobacilus fermentum757
Lacticaseibacillus rhamnosus892
Lactobacillus acidophilus875
Lactobacillus paracasei573
Lactobacillus casei56-
Limosilactobacillus reuteri431
Levilactobacillus brevis541
Lactobacillus salivarius3-1
Lactobacillus helveticus23-
Lactobacillus delbrueckii12-
Lactobacillus crispatus122
Lactobacillus pentosus121
Lactobacillus curvatus111
Lactobacillus caucasicus111
Other Lactobacillaceae20256
Bacillus subtilis321
Bacillus cereus111
Other Bacillus spp.421
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Neidhöfer, C.; Rathore, K.; Parčina, M.; Sieber, M.A. ESKAPEE Pathogen Biofilm Control on Surfaces with Probiotic Lactobacillaceae and Bacillus species. Antibiotics 2023, 12, 871. https://doi.org/10.3390/antibiotics12050871

AMA Style

Neidhöfer C, Rathore K, Parčina M, Sieber MA. ESKAPEE Pathogen Biofilm Control on Surfaces with Probiotic Lactobacillaceae and Bacillus species. Antibiotics. 2023; 12(5):871. https://doi.org/10.3390/antibiotics12050871

Chicago/Turabian Style

Neidhöfer, Claudio, Kamni Rathore, Marijo Parčina, and Martin A. Sieber. 2023. "ESKAPEE Pathogen Biofilm Control on Surfaces with Probiotic Lactobacillaceae and Bacillus species" Antibiotics 12, no. 5: 871. https://doi.org/10.3390/antibiotics12050871

APA Style

Neidhöfer, C., Rathore, K., Parčina, M., & Sieber, M. A. (2023). ESKAPEE Pathogen Biofilm Control on Surfaces with Probiotic Lactobacillaceae and Bacillus species. Antibiotics, 12(5), 871. https://doi.org/10.3390/antibiotics12050871

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop