African Journal of
Microbiology Research

  • Abbreviation: Afr. J. Microbiol. Res.
  • Language: English
  • ISSN: 1996-0808
  • DOI: 10.5897/AJMR
  • Start Year: 2007
  • Published Articles: 5233

Review

Probiotics Lactobacillus strains: A promising alternative therapy against to biofilm-forming enteropathogenic bacteria?

Mariane Silveira Magalhães Fernandes
  • Mariane Silveira Magalhães Fernandes
  • Laboratory of Biofilms and Antimicrobial Agents – LABAM, Faculty of Medicine, Federal University of Ceará (UFC), Brazil.
  • Search for this author on:
  • Google Scholar
Maria Leilah Monte Coelho Lourenço
  • Maria Leilah Monte Coelho Lourenço
  • Laboratory of Biofilms and Antimicrobial Agents – LABAM, Faculty of Medicine, Federal University of Ceará (UFC), Brazil.
  • Search for this author on:
  • Google Scholar
Brendda Miranda Vasconcelos
  • Brendda Miranda Vasconcelos
  • Laboratory of Bioprospecting and Applied Molecular Experimentation – NUBEM, University Center INTA (UNINTA), Brazil.
  • Search for this author on:
  • Google Scholar
Victor Alves Carneiro
  • Victor Alves Carneiro
  • Laboratory of Biofilms and Antimicrobial Agents – LABAM, Faculty of Medicine, Federal University of Ceará (UFC), Brazil.
  • Search for this author on:
  • Google Scholar


  •  Received: 12 June 2019
  •  Accepted: 24 September 2019
  •  Published: 31 October 2019

 ABSTRACT

Biofilms formation stands out in context of persistent intestinal infections caused by Enterobacteriaceae, which are associated with a high resistance to antimicrobial agents’ and phagocytosis by host defense cells. Hence, understanding the mechanisms involved in this process becomes major for the development of new preventive and therapeutic strategies. Lactic acid bacteria, including species of the genus Lactobacillus, have been associated with the prevention or dispersion of biofilms formed by pathogenic microorganisms. This effect is often associated with the antimicrobial substances production, among them organic acids, bacteriocins, hydrogen peroxide and biorsurfactants. However, the antibiofilm action of Lactobacillus seems to be strain-specific and may not be demonstrated by strains of the same genus. Thus, diet supplementation with beneficial microorganisms represents a possible strategy for prevention and treatment of intestinal infectious diseases, such as persistent or acute diarrhea caused by enteropathogenic bacteria. However, in vitro and in vivo further studies are needed to clarify the efficacy of different probiotic candidates, including commercially available products.

 

Keyword: Enterobacteria, biofilm, lactobacillus, antimicrobials.


 INTRODUCTION

The term biofilm describes a lifestyle characterized by microbial adhesion with production of extracellular polymer substances, constituting a gelatinous network that protects the cells and its associated with numerous cases of infections in human beings (Schiebel et al., 2017). In a liquid environment the primary event of biofilm formation, mainly in Gram-negative bacteria such as Escherichia coli and Salmonella, is related to the flagellar apparatus, which provide an initial approach between the bacterial cell and the surface (Misselwitz et al., 2012; Guttenplan and Kearns, 2013). Afterwards, three sequential steps, initial microbial adhesion, attachment either by exopolysaccharide production and cell surface structures, and colonization by growth of attached organisms, guarantee their survival in complex environments (Tolker-Nielsen, 2015).
 
 
The biofilm formation is considered as an essential factor in the pathogenesis of various enteropathogenic bacteria such as enteroaggregative E. coli (EAEC), which has been frequently implicated with several kinds of diarrhea (Meng et al., 2011; Dallman et al., 2012; Lääveri et al., 2014; Bamidele et al., 2019). Thus, diseases related with the ability of bacteria to form a structured microbial community are generally difficult to treat due to intrinsic biofilm resistance against antimicrobial agents (Haney et al., 2018; Bjarnsholt et al., 2013). In the attempt to explore new forms that may contribute to the prevention and treatment of infectious intestinal diseases, probiotics are standing out in merit of their protective effect against bacterial pathogens (Ramos et al., 2012; Sikorska and Smoragiewicz, 2013; Osama et al., 2017). Lactic acid bacteria (LAB), including Lactobacillus species, have been associated with the prevention or dispersion of biofilms formed by enteropathogenic microorganisms (Kaur et al., 2018; Miquel et al., 2016). Therefore, this review aims to describe the biotechnological application of Lactobacillus strains as probiotic agents and their role to counteract with enteropathogenic microbial biofilms, which may represent a promising alternative therapy.
 
Infectious intestinal diseases and enteropathogens
 
There is a complex beneficial relationship in intestine environment between host and gut microbiota that seeks a homeostatic equilibrium in which both are favored (Paixão and Castro, 2016). Thus, the interruption of this synchrony may result in the prevalent growth of pathogenic microorganisms, causing tissue inflammation and immunological regulation failures (Iacob et al., 2019). The ingestion of contaminated food or water are among the various causes of intestinal dysbiosis (Gabliardi et al., 2018). Food-borne outbreaks caused by several Enterobacteriaceae have been reported in Brazil, with emphasis on classical microorganisms such as E. coli and Salmonella sp. (Feltes et al., 2017).
 
Although many microorganisms cause foodborne infections, the severity of the disease, clinical manifestations, and duration of symptoms differ significantly (AL-Mamun et al., 2018). For instance, Vibrio cholerae and some strains of E. coli are capable to induce secretory diarrhea by exotoxins production (Choi et al., 2016; Chau et al., 2016; Chen et al., 2019). It triggers the intracellular cAMP and cGMP levels and result in the activation of the cyclic transmembrane conductance regulator nucleotide (CFTR) of Cl- channels, increasing fluid secretion into intestinal lumen (Thiagarajah et al., 2015). Furthermore, the high production of cAMP, cGMP and Ca2+ by host cells induced through enterotoxins inhibits the sodium-hydrogen antiporter (NHE3), which is the main exchanger channel responsible for maintaining of cellular sodium balance (Beltrán et al., 2015; Hodges and Gill, 2010).
 
On the other hand, bacteria such as Campylobacter jejuni, Shigella spp. and enteric Salmonella invade epithelial cells and trigger a massive neutrophilic infiltrate into the mucosa, followed by cellular transmigration into intestinal lumen (Navaneethan and Giannella, 2008). Thus, a response is established with recruitment of immune cells and release of cytokines, which characterizes inflammatory diarrhea (Hodges and Gill, 2010). It should be noted that enteropathogenic bacteria also alter the expression of transport proteins, as well, influencing the absorption of Na+ and Cl- (Marchelletta et al., 2013).
 
Intestinal microbiota may act as a very competitive environment, since it can host over 2000 bacterial species (Novik and Savich, 2019). However, high nutrients availability combined with a constant microorganisms’ influx makes the gastrointestinal environment ideal for development of sessile communities by enteropathogens, called biofilms, fact closely related to chronic intestinal infections (Rosenvinge et al., 2016). Biofilm formation represents an ability developed by the most microorganisms, which facilitates colonization on new surfaces with increased tolerance to environmental stresses (Miquel et al., 2016). Thus, the morphology, cellular density, as well as their physiological state are associated to wide range of antibiotic resistance (Singh et al., 2017).
 
The development of the biofilm starts from a response of the planktonic cells to environmental signals in order to raise survival chances, altering the expression of hundreds of genes (Oliveira et al., 2015). In short, this process begins by the cell attachment to (a)biotic surface, reversibly adhered. Then, irreversibly attachment happens after cell proliferation with microcolonies formation, and polymer matrix production. Finally, maturation is achieved, followed by detachment or dispersion of mature biofilm parts, which may determine the appearance of cellular clusters on new colonization sites (Tolker-Nielsen, 2015).
 
External bacterial structures play an important role in biofilms formation by enteropathogens, which may include fimbriae, flagella and capsules (Rabin et al., 2015). The first one stands out for facilitating bacterial aggregation and adhesion on several substrates, being very common in Gram-negative organisms. These cellular interactions are also triggered by the presence of specific components encoded by plasmids, such as adhesins and curli, potent inducers of the inflammatory response in the host (Wolska et al., 2016).
 
Genetic mechanism directly influences the ability to form cell agglomerates and, consequently, the pathogenesis of each bacterial species (Wolska et al., 2016). Schiebel et al. (2017) related the expression of fimH and agn43 genes in pathogenic E. coli strains with the ability to form biofilms by encoding type 1 fimbriae and Ag43 antigen. It is known that adhesins are essential for   initial   cell   adhesion  on  the  surface  and  Ag43  is capable of promoting auto cell-to-cell aggregation (Schiebel et al., 2017). Nascimento et al. (2014) also associate the participation of type 1 fimbriae with strong biofilm production by enteropathogenic E. coli strains (EPEC). Also in EPEC isolates, bundle-forming pilus (BFP) and the EspA filament are involved in the formation of microcolonies on epithelial cells and abiotic surfaces (Saldaña et al., 2009 and Moreira et al., 2006).


 PROBIOTICS MICROORGANISMS

Probiotics are living microorganisms that, when administrated in adequate amounts, confer a health benefit on the host, and can be found in foods or as dietary supplements and medications (WHO, 2002; Hill et al., 2014). The most commonly used are those belonging to Lactobacillus and Bifidobacterium genus, which are commensals bacteria that live in or on human bodies (Chew et al., 2015; Novik and Savich, 2019). Currently, the main claim for use of probiotic bacteria are: helping healthy microbiota maintenance, reducing the numbers or colonization of pathogenic bacteria, promoting the digestion of lactose by intolerant individuals, relieving constipation and increasing the absorption of vitamins and minerals (Novik and Savich, 2019). In addition, due to evidence of antimicrobial effect against several pathogens, the interest on the metabolic performance of these organisms has increased in recent years (Abdelhamid et al., 2018; Do Carmo et al., 2018; Osama et al., 2017).
 
Probiotics strains can affect pathogenic microorganisms through different mechanisms, such as enhancing the intestinal barrier function, increasing mucin production and modulating the immune system activity (Miquel et al., 2016; Hu et al., 2017; Vieco-Saiz et al., 2019). Other factors such as metabolites production, nutrients competition and suppression of toxin production are also involved in probiotic action (Markowiak and Slizewska, 2017). All of those effects can be triggered by metabolites, cell wall components, DNA fragments, as well as the adhesion of probiotic cells to host epithelium (Oelschlaeger, 2010).
 
Recent in vitro studies concluded that the use of LABs, specially Lactobacillus species, are related to positive results against enteropathogens (Turková et al., 2013; Ruiz et al., 2017; Prabhurajeshwar and Chandrakanth, 2017; Kaur et al., 2018). However, when it comes to clinical trials, the effects against bacterial infections are related to regular consumption of food sources, such as yogurts and curds, as well as supplementation (Varavallo et al., 2008; Halder and Mandal, 2016; Prabhurajeshwar and Chandrakanth, 2017).
 
Other effect associated to probiotics strains is the inhibition of virulence-related gene expression, such as toxins production (Rätsep et al., 2017). Thus, the efficacy of certain strains for the treatment of diarrheal diseases is probably associated with their ability to protect the host against toxins action, including those produced by cyanobacteria and fungi (Oelschlaeger, 2010). Carey et al. (2008) reported that 15 different Lactobacillus strains were able to inhibit the expression of shiga-toxin production by EHEC O157:H7, from the production of organic acids in sub-bactericidal concentrations with consequent pH reduction. Rätsep et al. (2017), testing the combination of xylitol with Lactobacillus plantarum detected the suppression of spores’ germination and outgrowth into vegetative toxin producing cells of C. difficile, which reduces the colonization of gut with the pathogen.
 
Enterobacteria and Lactobacillus Interactions
 
Lactobacillus genus corresponds to an important group of microorganisms related to ferment dairy products, as starters or as secondary microbiota, as well as food preservation (Ruiz et al., 2017). Several species of this group have been accepted with GRAS (Generally Recognized as Safe) status, which identifies a microorganism or microbial derivatives as safe for use in food industry (Cui et al., 2017; Gabliardi et al., 2018). Lactobacillus is frequently found in environments with low molecular oxygen tension, such as intestinal and urinary tract of humans, sharing their habitat with several types of potentially pathogenic microorganisms, among them pathogenic enterobacteria (WGO, 2017; Ruiz et al., 2017). Thus, these microorganisms have antagonistic properties against to pathogenic bacteria through metabolites production that render a hostile environment, such as organic acids, hydrogen peroxide, biosurfactants and bacteriocins (Fijan, 2014; Davoodabadi et al., 2015; Yeganeh et al., 2017; Abdelhamid et al., 2018; Fernandes, 2019; Vieco-Saiz et al., 2019).
 
Although lactic and/or acetic acids are considered to have low acidity, it is noteworthy the bactericidal effect against numerous pathogens, especially under conditions with nutrient limitation (Fijan, 2014). In these conditions, acids in the non-dissociated form penetrate the cytoplasm, where they dissociate and decrease the intracellular pH, interfering on cellular metabolic processes (Hughes and Webber, 2017). In addition, these acids increase the permeability of the outer membrane of Gram-negative organisms, compromising their integrity, what may potentiate the action of other antimicrobial substances such as bacteriocins (Gálvez et al., 2010). Hydrogen peroxide produced by many strains of Lactobacillus is also capable of inducing stresses in the outer membrane of some bacteria, such as uropathogenic E. coli (UPEC) which affects the structure of fimbriae and prevent their cell adhesion ability (Costa et al., 2012).
 
In addition, Halder and Mandal (2016) have shown that Lactobacillus  from  different  species,   individually,  have demonstrated excellent in vitro inhibition of enterobacteria growth, such as E. coli and K. pneumoniae. Also, when tested different strains combination from the same genus, they showed a synergistic effect against E. coli (Halder and Mandal, 2016). The use of isolated species, as well as blends containing different strains combined have been shown to be useful in the treatment of gastrointestinal diseases in vivo (Vuotto et al., 2014). Nevertheless, bactericidal capacity does not necessarily predict an antibiofilm action (Kaur et al., 2018). Considering the increasing ability of pathogens to generate persistent infections related to biofilms formation, probiotics administration may be able to modulate and prevent the proliferation of invasive microorganisms in vivo (Vuotto et al., 2014).
 
Antibiofilm strategies
 
The trend in health promotion through natural means leads to interest in non-chemical antibiotic agents, including microbial products, capable of reducing bacterial biomass (Challinor and Bode, 2015; Miquel et al., 2016). Two mechanisms are verified to be able of modulating the formation of these communities: destabilization of mature biofilms irreversibly attached or the inhibition of bacterial surface attachment (Miquel et al., 2016). In this perspective, in vitro and in vivo studies shown that probiotics are useful to modify the composition of the exopolymeric matrix, affecting the primary cell adhesion and/or colonization by exclusion/competition, or even trigger a cellular dispersion from biofilm (Gutiérrez et al., 2016).
 
Recent researches highlight the antibiofilm feature of Lactobacillus genus. Osama et al. (2017) demonstrated antimicrobial and antibiofilm action of Lactobacillus rhamnosus and Lactobacillus gasseri strains against Pseudomonas aeruginosa, E. coli and Staphylococcus aureus, three pathogens commonly involved in persistent infections associated with biofilm formation. As also, Abdelhamid et al. (2018) identified effective results in the biofilm eradication from multidrug resistant (MDR) E. coli isolates through bioactive compounds acting as antimicrobials. Fernandes (2019) demonstrated that cell free supernatant produced by standard and commercial probiotic strains (L. acidpohillus LA14, L. acidophillus ATCC 4356 and L. rhamnosus ATCC 9595) exerted strong bactericidal and antibiofilm action against MDR E. coli isolated from fish fillet samples.
 
However, the results obtained are attributed to several mechanisms of action which requires further investigations. For instance, an effective strategy to avoid the first step of biofilm formation it’s through to biosurfactants use, that impairs microbial adhesion modifying the physicochemical cell surface properties (Gómez et al., 2016; Sharman and Saharan, 2016; Kaur et al., 2018). The  antibiofilm  activity is also related to the production of bacteriocins, which are antimicrobial peptides produced by certain bacteria, that act suppressing biofilm formation and have a high applicability as food bioconservatives, since they have a broad spectrum against many food spoilage microorganisms, among them E. coli (Mathur et al., 2017; Novik and Savich, 2019).
 
The most of bacteriocins secreted by Lactobacillus belong to class II, heat stable, whose effect is related to the membrane destabilization with pores formation, plasma content extravasation and consequent cell death (Paixão and Castro, 2016). It is already recognized that bacteriocins action is potentiated under acidic conditions, which highlights the importance of organic acids secreted by various probiotic strains (Gálvez et al., 2010). The assembly of these antimicrobial peptides is controlled according to population density and communication between the cells through Quorum Sensing (QS), a process that bacteria use to coordinate gene expression and allow the production of virulence factors (Lixa et al., 2015).
 
QS control has become one of the purposes in the development of new strategies for the treatment of bacterial biofilm infections (Wu et al., 2015). Through QS, bacteria tend to produce low molecular weight chemical signals called autoinducers (AIs) that, when diffusing into the medium might be internalized to induce the differential genes expression that alter cellular metabolism (Lixa et al., 2015). Several enterobacteria are recognized for producing and responding to these AIs, so they can express virulence factors, succeed in colonization, and consequently to establish intestinal infections. Therefore, the use of probiotics emerges also due to produce small biologically active molecules capable of interfering on bacterial pathogens QS (Li et al., 2011; Liu et al., 2016). Some elucidations about the main mechanisms of action by Lactobacillus strains are able to exert an antibiofilm action are summarized in Table 1.
 
 
Although numerous in vitro evidences about antimicrobial activity of Lactobacillus strains, relevant actions of these probiotic preparation have been also observed by classical in vivo infectious models, as bacterium- and/or rotavirus-infected animals (Nakazato et al., 2011; Quigley et al., 2019; Jiang et al., 2017; Vlasova et al., 2013; Zhang et al., 2013). Normally, the probiotics effects have been related to normalization of intestinal microbial communities, competitive exclusion of pathogens associated with gut epithelia, bacteriocin production, production of short-chain fatty acids and modulation the activity of the immune system (Plaza-Diaz et al., 2019). Therefore, investigations performed by in vivo models are strongly recommended to help in the clarification of the mechanisms of action by each probiotic candidate.
 
In human beings, probiotic Lactobacillus strains can survive after oral  administration  and  efficiently  colonize  different parts of gastrointestinal tract, but the maintenance of the strain into gut environment seems to depends on intake frequency of probiotic preparation (Saxelin et al., 2010; Balgir et al., 2013; Arioli et al., 2018; Taverniti et al., 2019). That may explain when some of these probiotic strains come to randomized clinical trials, the results are occasionally inconclusive, and these intriguing outcomes put on doubt the clinical value of this treatment method (Chau et al., 2018; Ten Bruggencate et al., 2015; Hegar  et  al.,  2015;  Piescik-Lech et al., 2013). However, it must be considered that the anti-infectious action of Lactobacillus is not equally effective for all disease prevention or treatment indication. Several factors are involved on efficacy of probiotic strains, among them adequate doses for appropriate periods, besides diseases type and mechanisms of action of strains (Liu et al., 2019; Islam, 2016; Floch et al., 2015). In other words, the correct choose of probiotic must be strain-specific, and should not be generalized even among strains into the same species (Sniffen et al., 2018; McFarland et al., 2018; Liu et al., 2018).
 
Meanwhile, it is worthy to highlight that those desirable effects trough probiotic administration encourage and indicate Lactobacillus species as promising therapy strategies against enteropathogens (Szajewska et al., 2016; Bustos and Chamorro, 2018). In the end, the real impact of probiotic administration on the microbial ecology of the gastrointestinal tract and on animal health is far from being understood (Ten Bruggencate et al., 2014; Suez et al., 2018). 


 CONCLUSION

In conclusion, the biotechnological application of Lactobacillus strains as probiotics presents effective results to control microbial biofilms formed by enteropathogenic bacteria, representing a promising alternative for medicine use. The inhibitory effect seems to be strain specific and is referred to metabolic compounds, such as organic acids, hydrogen peroxide, bacteriocins, biosurfactants and QS inhibitors. Although, in vitro activity does not always correspond to in vivo results, which shows that further clinical trials are needed to predict select real beneficial strains.

 


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.

 


 ACKNOWLEDGMENT

The authors show gratitude to the institutions University Center INTA and Federal University of Ceara for support during the course of this research.



 REFERENCES

 

Abdelhamid AG, Esaam A, Hazaa MM (2018). Cell free preparations of probiotics exerted antibacterial and antibiofilm activities against multidrug resistant E. Coli. Saudi Pharmaceutical Journal 26(5):603-607.
Crossref
 

AL-Mamun M, Chowdhury T, Biswas B, Absar N (2018). Food poisoning and intoxication: A global leading concern for human health. Food Safety and Preservation pp. 307-352.
Crossref

  
 

Arioli S, Koirala R, Taverniti V, Fiore W, Guglielmetti S (2018). Quantitative recovery of viable Lactobacillus paracasei CNCM I-1572 (L. casei DG®) after gastrointestinal passage in healthy adults. Frontiers in Microbiology 9:1720.
Crossref

  
 

Balgir PP, Kaur B, Kaur T, Daroch N, Kaur G (2013). In vitro and in vivo survival and colonic adhesion of Pediococcus acidilactici MTCC5101 in human gut. BioMed research international 2013:1-9.
Crossref

  
 

Bamidele O, Jiang ZD, Dupont H (2019). Occurrence of putative virulence-related genes, aatA, aggR and aaiC, of Enteroaggregative Escherichia coli (EAEC) among adults with travelers' diarrhea acquired in Guatemala and Mexico. Microbial pathogenesis 128:97-99.
Crossref

  
 

Beltrán AR, Carraro-Lacroix LR, Bezerra CN, Cornejo M, Norambuena K,Toledo F, Araos J, Pardo F, Leiva A, Sanhueza C, Malnic G, Sobrevia L, Ramírez MA (2015). Escherichia coli heat-stable enterotoxin mediates Na+/H+ exchanger 4 inhibition involving cAMP in T84 human intestinal epithelial cells. PLoS One. 10(12):e0146042.
Crossref

  
 

Bjarnsholt T, Ciofu O, Molin S, Givskov M, Hoiby N (2013). Applying insights from biofilm biology to drug development-can a new approach be developed?. Nature Reviews Drug Discovery 12(10):791-808.
Crossref

  
 

Bustos SP, Chamorro JFV (2018). Probiotics in Acute, Antibiotic-associated and Nosocomial Diarrhea: Evidence in Pediatrics. Revista Colombiana de Gastroenterologia 33(1):41-48.
Crossref

  
 

Carey CM, Kostrzynska M, Ojha S, Thompson S (2008). The effect of probiotics and organic acids on Shiga-toxin2 gene expression in enterohemorrhagic Escherichia coli O157:H7. Journal of Microbiological Methods 73(2):125-132.
Crossref

  
 

Challinor VL, Bode HB (2015). Bioactive natural products from novel microbial sources. Annals of the New York Academy of Sciences 1354(1):82-97.
Crossref

  
 

Chau ML, Hartantyo SH, Yap M, Kang JS, Aung KT, Gutiérrez RA, Ng LC, Tam CC, Barkham T (2016). Diarrheagenic pathogens in adults attending a hospital in Singapore. BMC Infectious Diseases 16: 32. 
Crossref

  
 

Chau TTH, Chau NNM, Le NTH, The HC, Vinh PV, To NTN, Ngoc NM, Tuan HM, Ngoc TLC, Kolader ME, Farrar JJ, Wolbers M, Thwaites GE, Baker S (2018). A double blind, randomized, placebo-controlled trial of Lactobacillus acidophilus for the treatment of acute watery diarrhea in vietnamese children. The Pediatric Infectious Disease Journal 37(1):35-42.
Crossref

  
 

Chen C, Wang LP, Yu JX, Chen X, Wang RN, Yang XZ, Zheng SF, Yu F, Zhang ZK, Liu SJ, Li ZJ, Chen Y (2019). Prevalence of enteropathogens in outpatients with acute diarrhea from urban and rural areas, southeast China, 2010-2014. American Journal of Tropical Medicine and Hygiene tpmd19-0171. 
Crossref

  
 

Chew SY, Cheah YK, Seow HF, Sandai D, Than LTL (2015). Probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 exhibit strong antifungal effects against vulvovaginal candidiasis-causing Candida glabrata isolates. Journal of Applied Microbiology 118(5):1180-1190.
Crossref

  
 

Choi SY, Rashed SM, Hasan NA, Alam M, Islam T, Sadique A, Johura F-T, Eppinger M, Ravel J, Huq A, Cravioto A, Colwell RR (2016). Phylogenetic diversity of Vibrio cholerae associated with endemic cholera in Mexico from 1991 to 2008. mBio 7(2):e02160-15.
Crossref

  
 

Costa GN, Suguimoto HH, Miglioranzaand LHS, Gómez RJHC (2012). Antimicrobial activity of Lactobacillus and Bifidobacterium strains against pathogenic microorganisms "in vitro". Semina: Ciencias Agrárias 33(5):1839-1846.
Crossref

  
 

Cui X, Shi Y, Gu S, Yan X, Chen H, Ge J (2017). Antibacterial and Antibiofilm Activity of Lactic Acid Bacteria Isolated from Traditional Artisanal Milk Cheese from Northeast China Against Enteropathogenic Bacteria. Probiotics and Antimicrobial Proteins 1-10.
Crossref

  
 

Dallman T, Smith GP, O'Brien B, Chattaway MA, Finlay D, Gran, KA, Jenkins C (2012). Characterization of a verocytotoxin-producing enteroaggregative Escherichia coli serogroup O111:H21 strain associated with a household outbreak in Northern Ireland. Journal of Clinical Microbiology 50(12):4116-4119.
Crossref

  
 

Das JK, Mishra D, Ray P, Tripathy P, Beuria TK, Singh N, Suar M (2013) In vitro evaluation of anti-infective activity of a Lactobacillus plantarum strain against Salmonella enterica serovar Enteritidis. Gut Pathogens 5(1):11.
Crossref

  
 

Davoodabadi A, Dallal MMS, Lashani E, Ebrahimi MT (2015). Antimicrobial activity of Lactobacillus spp. isolated from fecal flora of healthy breast-fed infants against diarrheagenic Escherichia coli. Jundishapur Journal of Microbiology 8(12).
Crossref

  
 

Do Carmo MS, Santos CI, Araújo MC, Girón JA, Fernandes ES, Monteiro-Neto V (2018). Probiotics, mechanisms of action, and clinical perspectives for diarrhea management in children. Food & Function 9(10):5074-5095.
Crossref

  
 

Feltes MMC, Arisseto-Bragotto AP, Block JM (2017). Food quality, food-borne diseases, and food safety in the Brazilian food industry. Food Quality and Safety 1(1):13-27.
Crossref

  
 

Fernandes MSM (2019). Atividade antimicrobiana e antibiofilme do sobrenadante de cepas de Lactobacillus cell-free sobre isolados de Escherichia coli farmacorresistentes. MS Thesis. Federal University of Ceará, CE, Brazil. 2019. 

View

  
 

Fijan S (2014). Microorganisms with Claimed Probiotic Properties: An Overview of Recent Literature. Journal of Environmental Research and Public Health 11(5):4745-4767.
Crossref

  
 

Floch MH, Walker WA, Sanders ME, Nieuwdorp M, Kim AS, Brenner DA, Qamar AA, Miloh TA, Guarino A, Guslandi M, Dieleman LA, Ringel Y, Quigley EM, Brandt LJ (2015). Recommendations for probiotic use - 2015 Update: Proceedings and consensus opinion. Journal of Clinical Gastroenterology 49(Suppl 1):S69-S73.
Crossref

  
 

Gabliardi A, Totino V, Cacciotti F, Iebba V, Neroni B, Bonfiglio G, Trancassini M, Passariello C, Pantanella F, Schippa S (2018). Rebuilding gut microbiota ecosystem. Journal of Environmental Research and Public Health 15(8):1679.
Crossref

  
 

Gálvez A, Abrioul H, Benomar N, Lucas R (2010). Microbial antagonists to food-borne pathogens and biocontrol. Current Opinion in Biotechnology 21(2):142-148.
Crossref

  
 

Gómez NC, Ramiro JM, Quecan BXV, Franco BGDM (2016). Use of potential probiotic lactic acid bacteria (LAB) biofilms for the control of Listeria monocytogenes, Salmonella typhimurium and Escherichia coli O157:H7 biofilms formation. Frontiers in Microbiology 7:863.
Crossref

  
 

Gutiérrez S, Martínez-blanco H, Rodríguez-Aparicio LB, Ferrero MA (2016). Effect of fermented broth from lactic acid bacteria oh pathogenic bacteria proliferation. Journal of Dairy Science 99(4): 2654-2665.
Crossref

  
 

Guttenplan SB, Kearns DB (2013). Regulation of flagellar motility during biofilm formation. FEMS Microbiology Reviews 37(6):849-871.
Crossref

  
 

Halder D, Mandal S (2016). Antibacterial potentiality of commercially available probiotic Lactobacilli and curd Lactobacilli strains, alone and in combination, against human pathogenic bacteria. Translational Biomedicine 7:1-7.
Crossref

  
 

Haney EF, Trimble MJ, Cheng JT, Vallé Q, Hancock REW (2018). Critical assessment of methods to quantify biofilm growth and evaluate antibiofilm activity of host defence peptides. Biomolecules 8(2) 29.
Crossref

  
 

Hegar B, Waspada IM, Gunardi H, Vandenplas Y (2015). A double blind randomized trial showing probiotics to be ineffective in acute diarrhea in Indonesian children. Indian Journal Pediatrics 82(5):410-414.
Crossref

  
 

Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminem S, Calder PC, Sanders AE (2014). The international scientific association for probiotics consensus statement on the scope and appropriate use of the term probiotic. Nature reviews Gastroenterology & Hepatology 11(8):506-514.
Crossref

  
 

Hodges K, Gill R (2010). Infectious diarrhea: cellular and molecular mechanisms. Gut Microbes 1(1):4-21.
Crossref

  
 

Hu S, Wang L, Jiang Z (2017). Dietary additive probiotics modulation of intestinal microbiota. Protein and Peptides Letters 24(5):382-387.
Crossref

  
 

Hughes G, Webber MA (2017). Novel approaches to the treatment of bacterial biofilm infections. British Journal of Pharmacology 174:2237-2246.
Crossref

  
 

Iacob S, Iacob DG and Luminos LM (2019). Intestinal Microbiota as a Host Defense Mechanism to Infectious Threats. Frontiers in Microbiology 9:3328.
Crossref

  
 

Islam SU (2016). Clinical uses of probiotics. Medicine 95(5):e2658.
Crossref

  
 

Jiang Y, Ye L, Cui Y, Yang G, Yang W, Wang J, Hu J, Gu W, Shi C, Huang H, Wang C (2017). Effects of Lactobacillus rhamnosus GG on the maturation and differentiation of dendritic cells in rotavirus-infected mice. Beneficial Microbes 8(4):645-656.
Crossref

  
 

Kaur S, Sharma P, Kalia N, Singh J, Kaur S (2018). Anti-biofilm properties of the fecal probiotic Lactobacilli against Vibrio spp. Frontiers in Cellular and Infection Microbiology 8:120.
Crossref

  
 

Lääveri T, Pakkanen SH, Antikainen J, Riutta J, Mero S, Kirveskari J, Kantele A (2014). High number of diarrhoeal coinfections in travellers to Benin, West Africa. BMC Infectious Diseases 14:81.
Crossref

  
 

Lagrafeuille R, Miquel S, Balastrino D, Vareille-Delarbre M, Chain F, Langella P, Forestier C (2018). Opposing effect of Lactobacillus on in vitro Klebsiella pneumoniae in biofilm and in an in vivo intestinal colonization model. Beneficial Microbes 9(1):87-100.
Crossref

  
 

Li J, Wang W, Xu SX, Magarvey NA, McCormick JK (2011). Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. Proceedings of the National Academy of Sciences 108(8):3360-3365.
Crossref

  
 

Liu J, Gu Z, Song F, Zhang H, Zhao J, Chen W (2019). Lactobacillus plantarum ZS2058 and Lactobacillus rhamnosus GG use different mechanisms to prevent Salmonella infection in vivo. Frontiers in Microbiology 10: 299. 
Crossref

  
 

Liu J, Hu D, Chen Y, Huang H, Zhang H, Zhao J, Gu Z, Chen W (2018). Strain-specific properties of Lactobacillus plantarum for prevention of Salmonella infection. Food and Function 9(7):3673-3682.
Crossref

  
 

Liu W, Ran C, Liu Z, Gao Q, Xu S, Ringø E, Myklebust R, Gu Z, Zhou Z (2016). Effects of dietary Lactobacillus plantarum and AHL lactonase on the control of Aeromonas hydrophila infection in tilapia. MicrobiologyOpen 5(4):687-699.
Crossref

  
 

Lixa C, Mujo A, Anobom CD, Pinheiro AS (2015). A structural perspective on the mechanisms of quorum sensing activation in bacteria. Anais da Academia Brasileira de Ciências 87(4):2189-2203.
Crossref

  
 

Marchelletta RR, Gareau MG, McCole DF, Okamoto S, Roel E, Klinkenberg R, Guiney DG, Fierer J, Barrett KE (2013). Altered expression and localization of ion transporters contribute to diarrhea in mice with Salmonella-induced enteritis. Gastroenterology 145(6):1358-1368.
Crossref

  
 

Markowiak P, Slizewska K (2017). Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9(9):1021.
Crossref

  
 

Mathur H, Field D, Rea1 MC, Cotter PD, Hill C, Ross RP (2017). Bacteriocin-antimicrobial synergy: A medical and food perspective. Frontiers in Microbiology 8:1205.
Crossref

  
 

McFarland LV, Evans CT, Goldstein EJC (2018). Strain-specificity and disease-specificity of probiotic efficacy: A systematic review and meta-analysis. Frontiers in Medicine 5:124.
Crossref

  
 

Mendellin-Peña MJ, Griffiths MW (2009). Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157:H7 colonization. Applied and Environmental Microbiology 75(4):1165-1172.
Crossref

  
 

Meng CY, Smith BL, Bodhidatta L, Richard SA, Vansith K, Thy B, Srijan A, Serichantalergs O, Mason CJ (2011). Etiology of diarrhea in young children and patterns of antibiotic resistance in Cambodia. The Pediatric Infections Diseases Journal 30(4):331-335.
Crossref

  
 

Miquel S, Lagrafeuille R, Souweine B, Forestier C (2016). Anti-biofilm Activity as a Health Issue. Frontiers in Microbiology 7:592.
Crossref

  
 

Misselwitz B, Barrett N, Kreibich S, Vonaesch P, Andritschke D, Rout S, Weidner K, Sormaz M, Songhet P, Horvath P, Chabria M, Vogel V, Spori DM, Jenny P, Hardt WD (2012). Near surface swimming of Salmonella typhimurium explains target-site selection and cooperative invasion. PLoS Pathogens 8(7):e1002810.
Crossref

  
 

Moreira CG, Palmer K, Whiteley M, Sircili MP, Trabulsi LR (2006). Bundle-forming Pili and EspA are involved in biofilm formation by Enteropathogenic Escherichia coli. Journal of Bacteriology 188(11):3952-3961.
Crossref

  
 

Nakazato G, Paganelli FL, Lago JC, Aoki FH, Mobilon C, Brocchi M, Stehling EG, Silveira WD (2011). Lactobacillus acidophilus decreases Salmonella typhimurium invasion in vivo. Journal of Food Safety 31:284-289.
Crossref

  
 

Nascimento HH, Silva LEP, Souza RT, Silva NP, Scaletsky ICA (2014). Phenotypic and genotypic characteristics associated with biofilm formation in clinical isolates of typical enteropathogenic Escherichia coli (aEPEC) strains. BMC Microbiology 14(1):184.
Crossref

  
 

Navaneethan U, Giannella RA (2008). Mechanisms of infectious diarrhea. Nature Reviews Gastroenterology & Hepatology 5(11):637-647.
Crossref

  
 

Novik G, Savich V (2019). Beneficial microbiota. Probiotics and pharmaceutical products in functional nutrition and medicine. Microbes and Infection In Press. 
Crossref

  
 

Oelschlaeger TA (2010). Mechanisms of probiotic action - A review. International Journal of Medical Microbiology 300(1):57-62.
Crossref

  
 

Oliveira NM, Martinez-Garcia E, Xavier J, Durham WM, Kolter R, Kim W, Foster KR (2015) Biofilm formation as a response to ecological competition. PLoS Biology 13(7):e1002191.
Crossref

  
 

Osama DM, Elkhatib WF, Tawfeik AM, Mohammad M (2017). Antimicrobial, antibiofilm and immunomodulatory activities of Lactobacillus rhamnosus and Lactobacillus gasseri against some bacterial pathogens. International Journal of Biotechnology for Wellness Industries 6(1):12-21.
Crossref

  
 

Paixão LA, Castro FFS (2016). A colonização da microbiota intestinal e sua influência na saúde do hospedeiro. Universitas: Ciências da Saúde 14(1):85-96.
Crossref

  
 

Piescik-Lech M, Urbanska M, Szajewska H (2013). Lactobacillus GG (LGG) and smectite versus LGG alone for acute gastroenteritis: a double-blind, randomized controlled trial. European Journal of Pediatrics 172(2):247-253.
Crossref

  
 

Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A (2019). Mechanisms of action of probiotics. Advances in Nutrition 10:S49-S66.
Crossref

  
 

Prabhurajeshwar C, Chandrakanth RK (2017). Probiotic potential of Lactobacilli with antagonistic activity against pathogenic strains: an in vitro validation for the production of inhibitory substances. Biomedical Journal 40(5):270-283.
Crossref

  
 

Quigley L, Coakley M, Alemayehu D, Rea MC, Casey PG, O'Sullivan Ó, Murphy E, Kiely B, Cotter PD, Hill C, Ross RP (2019). Lactobacillus gasseri APC 678 reduces shedding of the pathogen Clostridium difficile in a murine model. Frontiers in Microbiology 10:273.
Crossref

  
 

Rabin N, Zheng Y, Opoku-Temeng C, Du Y, Bonsu E, Sintim HO (2015). Biofilm formation mechanisms and targets for developing antibiofilm agents. Future Medicinal Chemistry 7(4):493-512.
Crossref

  
 

Ramos AN, Sesto Cabral ME, Noseda D, Bosch A, Yantorno OM, Valdez JC (2012). Antipathogenic properties of Lactobacillus plantarum on Pseudomonas aeruginosa: The potential use of its supernatants in the treatment of infected chronic wounds. Wound Repair and Regeneration 20(4):552-562.
Crossref

  
 

Rätsep M, Kõljalg S, Sepp E, Smidt I, Truusalu K, Songisepp E, Stsepetova J, Naaber P, Mikelsaar RH, Mikelsaar M (2017). A combination of the probiotic and prebiotic product can prevent the germination of Clostridium difficile spores and infection. Anaerobe 47:94-103.
Crossref

  
 

Rosenvinge EC, Maldarelli GA, Piepenbrink KH, Scott AJ, Freiberg JA, Song Y, Achermann Y, Ernst RK, Shirtliff ME, Sundberg EJ, Donnenberg MS (2016). Type IV pili promote early biofilm formation by Clostridium difficile. FEMS Pathogens and Disease 74(6):ftw061.
Crossref

  
 

Ruiz MJ, Colello R, Padolaand NL, Etcheverría AI (2017). Efecto inhibitorio de Lactobacillus spp. sobre bactérias implicadas em enfermidades transmitidas por alimentos. Revista Argentina de Microbiologia 49(2):174-177.
Crossref

  
 

Saldaña Z, Erdem AL, Schüller S, Okeke IN, Lucas M, Sivananthan A, Phillips AD, Kaper JB, Puente JL, Girón JA (2009). The Escherichia coli common pilus and the bundle-forming pilus act in concert during the formation of localized adherence by enteropathogenic E. coli. Journal of Bacteriology 191(11):3451-3461.
Crossref

  
 

Sambanthamoorthy K, Feng X, Patel R, Patel S, Paranavitana C (2014). Antimicrobial and antibiofilm potential of biosurfactants isolated from lactobacilli against multi-drug-resistant pathogens. BMC Microbiology 14(1):197.
Crossref

  
 

Saxelin M, Lassig A, Karjalainen H, Tynkkynen S, Surakka A, Vapaatalo H, Järvenpää S, Korpela R, Mutanen M, Hatakka K (2010). Persistence of probiotic strains in the gastrointestinal tract when administered as capsules, yoghurt, or cheese. International Journal of Food Microbiology 144(2):293-300.
Crossref

  
 

Schiebel J, Böhm A, Nitschke J, Burdukiewicz M, Weinreich J, Ali A, Roggenbuck D, Rödiger S, Schierack P (2017). Genotypic and phenotypic characteristics associated with biofilm formation by human clinical Escherichia coli isolates of different pathotypes. Applied Environmental Microbiology 83(24):e01660-17.
Crossref

  
 

Sharman D, Saharan BS (2016). Functional characterization of biomedical potential of biosurfactant produced by Lactobacillus helveticus. Biotechnology Reports 11:27-35. 
Crossref

  
 

Sikorska H, Smoragiewicz W (2013). Role of probiotics in the prevention and treatment of meticillin-resistant Staphylococcus aureus infections. International Journal of Antimicrobial Agents 42(6):475-481.
Crossref

  
 

Singh S, Singh SK, Chowdhury I, Singh R (2017). Understanding the Mechanism of Bacterial Biofilms Resistance to Antimicrobial Agents. The Open Microbiology Journal 11:53-62.
Crossref

  
 

Sniffen JC, McFarland LV, Evans CT, Goldstein EJC (2018). Choosing an appropriate probiotic product for your patient: An evidence-based practical guide. PLoS One 13(12):e0209205.
Crossref

  
 

Suez J, Zmora N, Zilberman-Schapira G, Mor U, Dori-Bachash M, Bashiardes S, Elinav E (2018). Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell 174(6):1406-1423.
Crossref

  
 

Szajewska H, Canani RB, Guarino A, Hojsak I, Indrio F, Kolacek S, Orel R, Shamir R, Vandenplas Y, Van Goudoever JB, Weizman Z (2016). Probiotics for the Prevention of Antibiotic-Associated Diarrhea in Children. Journal of Pediatric Gastroenterology and Nutrition 62(3):495-506.
Crossref

  
 

Taverniti V, Koirala R, Via AD, Gargari G, Leonardis E, Arioli S, Guglielmetti S (2019). Effect of cell concentration on the persistence in the human intestine of four probiotic strains administered through a multispecies formulation. Nutrients 11(2):285.
Crossref

  
 

Ten Bruggencate SJ, Girard SA, Floris-Vollenbroek EG, Bhardwaj R, Tompkins TA (2015). The effect of a multi-strain probiotic on the resistance toward Escherichia coli challenge in a randomized, placebo-controlled, double-blind intervention study. European Journal of Clinical Nutrition 69:385-391.
Crossref

  
 

Ten Bruggencate SJM, Girard SA, Floris-Vollenbroek EGM, Bhardwaj R, Tompkins TA (2014). The effect of a multi-strain probiotic on the resistance toward Escherichia coli challenge in a randomized, placebo-controlled, double-blind intervention study. European Journal of Clinical Nutrition 69(3):385-391.
Crossref

  
 

Thiagarajah JR, Donowirtz M, Verkman AS (2015). Secretory diarrhoea: mechanisms and emerging therapies. Nature Reviews Gastroenterology & Hepatology 12(8):446-457.
Crossref

  
 

Tolker-Nielsen T (2015). Biofilm Development. Microbiology Spectrum 3(2):MB-0001-2014.
Crossref

  
 

Turková K, Mavric A, Narat M, Rittich B, Spanova A, Rogelj I, Matijasic BB (2013). Evaluation of Lactobacillus strains for selected probiotic properties. Folia Microbiologica 58(4):261-267.
Crossref

  
 

Vacheva A, Gerogieva R, Danova S, Mihova R, Marhova R, Kostadinova S, Vasileva K, Bivolarska M, Stoitsova SR (2012). Modulation of Escherichia coli biofilm growth by cell-free spent cultures from lactobacilli. Central European Journal of Biology 7(2):219-229.
Crossref

  
 

Varavallo MA, Thomé JN, Teshima E (2008). Aplicação de bactérias probióticas para profilaxia e tratamento de doenças gastrointestinais. Semina: Ciências Biológicas e da Saúde 29(1):83-104.
Crossref

  
 

Vieco-Saiz N, Belguesmia Y, Raspoet R, Auclair E, Gancel F, Kempf I, Drider D (2019). Benefits and inputs from lactic acid bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Frontiers in Microbiology 10:57.
Crossref

  
 

Vlasova AN, Chattha KS, Kandasamy S, Liu Z, Esseili M, Shao L, Rajashekara G, Saif LJ (2013). Lactobacilli and Bifidobacteria promote immune homeostasis by modulating innate immune responses to human rotavirus in neonatal gnotobiotic pigs. PLoS One 8(10):e76962.
Crossref

  
 

Vuotto F, Longo F, Donelli G (2014). Probiotics to counteract biofilm-associated infections: promising and conflicting data. International Journal of Oral Science 6(4):189-194.
Crossref

  
 

Wolska KI, Grudniak AM, Rudnicka Z, Markowska K (2016). Genetic control of bacterial biofilms. Journal of Applied Genetics 57(2):225-238.
Crossref

  
 

World Gastroenteroly Organisation (WGO) (2017). World Gastroenterology Organization Global Guidelines - Probiotics and Prebiotics. 

  
 

World Health Organization (WHO) (2002). Guidelines for the Evaluation of Probiotics in Food. Londres. 

  
 

Wu H, Moser C, Wang Q, Hoiby N, Song Z (2015). Strategies for combating bacterial biofilm infections. International Journal of Oral Science 7(1):1-7.
Crossref

  
 

Yeganeh M, Hosseini H, Mehrabian S, Torbatti ES, Zamir AM (2017). Antibiofilm effects of lactobacilli against ciprofloxacin-resistant uropathogenic Escherichia coli strains in pasteurized milk. Applied Food Biotechnology 4(4):241-250.

  
 

Zhang Z, Xiang Y, Li N, Wang B, Ai H, Wang X, Huang L, Zheng Y (2013). Protective effects of Lactobacillus rhamnosus GG against human rotavirus-induced diarrhoea in a neonatal mouse model. Pathogens and Disease 67(3):184-191.
Crossref

  
 

 




Copyright © 2024 Author(s) retain the copyright of this article.

This article is published under the terms of the Creative Commons Attribution License 4.0

Back to Vol. 13 No. 28
Back to articles
SUBSCRIBE TO RSS
SUBMIT MANUSCRIPT
CONFERENCES
          */?>