Implications and Mechanisms of Antiviral Effects of Lactic Acid Bacteria: A Systematic Review

Farahmandi, Fargol; Parhizgar, Parynaz; Mozafari Komesh Tape, Parya; Bizhannia, Fahimeh; Rohani, Fateme Sadat; Bizhanzadeh, Marzieh; Mostafavi Alhosseini, Zeinab Sadat; Hosseinzade, Maede; Farsi, Yeganeh; Nasiri, Mohammad Javad

doi:https://doi.org/10.1155/2023/9298363

International Journal of Microbiology

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Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Disclosure Conflicts of Interest Authors’ Contributions References Copyright Related Articles

Review Article | Open Access

Volume 2023 | Article ID 9298363 | https://doi.org/10.1155/2023/9298363

Implications and Mechanisms of Antiviral Effects of Lactic Acid Bacteria: A Systematic Review

Fargol Farahmandi,¹Parynaz Parhizgar,¹Parya Mozafari Komesh Tape,¹Fahimeh Bizhannia,¹Fateme Sadat Rohani,¹Marzieh Bizhanzadeh,¹Zeinab Sadat Mostafavi Alhosseini,¹Maede Hosseinzade,¹Yeganeh Farsi,¹and Mohammad Javad Nasiri²

Academic Editor: Karl Drlica

Received23 Apr 2023

Revised09 Oct 2023

Accepted17 Nov 2023

Published12 Dec 2023

Abstract

Background. Lactic acid bacteria (LAB) are among the most important strains of probiotics. Some are normal flora of human mucous membranes in the gastrointestinal system, skin, urinary tract, and genitalia. There is evidence suggesting that LAB has an antiviral effect on viral infections. However, these studies are still controversial; a systematic review was conducted to evaluate the antiviral effects of LAB on viral infections. Methods. The systematic search was conducted until the end of December 17, 2022, using international databases such as Scopus, Web of Science, and Medline (via PubMed). The keywords of our search were lactic acid bacteria, Lactobacillales, Lactobacillus (as well as its species), probiotics, antiviral, inhibitory effect, and virus. Results. Of 15.408 potentially relevant articles obtained, 45 eligible in-vivo human studies were selected for inclusion in the study from databases, registers, and citation searching. We conducted a systematic review of the antiviral effects of the LAB based on the included articles. The most commonly investigated lactobacillus specie were Lactobacillus rhamnosus GG and Lactobacillus casei. Conclusion. Our study indicates that 40 of the selected 45 of the included articles support the positive effect of LAB on viral infections, although some studies showed no significant positive effect of LABs on some viral infections.

1. Introduction

Viral infections have long been of great concerns, and emerging life-threatening viral infections during recent years have highlighted their importance [1]. Notable costs of treatment, considerable morbidity and mortality, and possible resistance to chemical drugs have led healthcare providers to seek alternative or adjuvant treatments to improve the cost-effectiveness of treatments and make them more available. Probiotics are among the most popular adjuvant treatments having proven effectiveness in a wide variety of diseases [2, 3].

Among probiotics, lactic acid bacteria (LAB) are among the well-studied bacteria, especially in recent years [4–6]. They are Gram-positive, non-spore-forming bacteria [7]. Some LABs exist as the normal flora of human and animal mucous membranes and colonize the gastrointestinal system (GI), skin, urinary tract, and genitalia [4]. LABs have several beneficial roles. In the GI tract, they reduce lactose intolerance, and they have antidiarrheal, anti-inflammatory, and antineoplastic activity [8]. As well, they have protective roles against peptic ulcers by eradicating H. pylori infection [9]. Modulation of immune responses and minimizing the allergic responses are their other beneficial effects [10, 11].

Growing evidence supports the antiviral, antibacterial, and antifungal effects of LABs [4, 5, 12]. Several mechanisms of antiviral activity have been proposed, both generally and specifically, according to certain viruses, but there is no conclusive research to establish the antiviral effects of LABs so far. The present study aims to systematically review the current literature on the antiviral effects of LABs and provide a comprehensive picture of it.

2. Materials and Methods

2.1. Search Strategy

This study was designed and performed to investigate the antiviral effects of LABs based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyzes (PRISMA) checklist [13].

The systematic search was conducted until the end of December 17, 2022, in Scopus, Web of Science, and Medline (via PubMed). The searched keywords were a combination of the following:

Lactic acid bacteria, Lactobacillales, Lactobacillus (as well as its species such as: Lactobacillus rhamnosus, Lactobacillus reuteri, Lactobacillus leichmannii, Lactobacillus helveticus, Lactobacillus fermentum, Lactobacillus brevis, Lactobacillus delbrueckii, Lactobacillus plantarum, Lactobacillus casei, Lactobacillus acidophilus, Lactobacillus sakei, Lactobacillus pentosus, Lactobacillus crispatus, Lactobacillus johnsonii, Lactobacillus gasseri, Lactobacillus salivarius, and Lactobacillus paracasei), probiotics, antiviral, inhibitory effect, virus.

2.2. Inclusion and Exclusion Criteria

All in-vivo original articles investigating the antiviral effects of LABs were considered eligible. Only studies written in English were included. Animal studies, in vitro studies, case reports, reviews, editorials, commentary, correspondence, and conference articles were excluded.

2.3. Study Selection

All search and screening steps were performed separately by two independent reviewers. The quality of articles included for data extraction was assessed by the Cochrane tool for experimental research and the Newcastle-Ottawa Scale (NOS) for observational studies [14, 15]. A third reviewer’s opinion was obtained in case of disagreement (shown in Tables 1 and 2).

The NOS scale assesses the likelihood of bias in prospective studies using the following three domains: participant selection, comparability, and results. A research may receive up to one point for each numbered item in the selection, two points for comparability, and up to two points for outcome categories. For poor, moderate, and excellent study quality, corresponding scores of 0–3, 4–6, and 7–9 were given.

The Cochrane tool is based on the following: the use of random sequence generation, concealment of condition allocation, blinding of participants and staff, blinding of outcome assessors, completeness of outcome data, and other biases. Each study was given a risk of bias rating: low when there was no worry, uncertain when there was no information, and high when there was concern.

2.4. Data Extraction

Two authors independently extracted the following variables from studies included in this review: the first author’s name, year of publication, type of study, the country of study execution, number of cases and controls, type of bacteria, type of virus, and antiviral effects of lactic acid bacteria on the virus (es).

3. Results

The study selection process is shown in Figure 1. According to the flowchart, 15,408 articles were obtained by the primary search. Due to duplication, 12,057 articles were excluded and the 3,337 remaining articles were screened.

In the next step, the title and abstract of the articles were screened in terms of being in vitro or in vivo, as well as the type of research article. Studies that seemed to be in vitro studies, case reports, reviews, editorials, commentary, correspondence, and conference articles were excluded (n = 3081). After screening the title and abstract, 256 articles remained for full-text screening. Ultimately, after exclusion of irrelevant and unavailable studies, 45 eligible articles were selected for full-text data extraction.

Of 45 included articles, 30 were randomized studies, 6 were cohorts, 7 were clinical trials, 1 case-control, and 1 placebo controlled crossover study.

Six of the included articles were conducted in Finland, six in Italy, four in Japan, three in the USA, three in Tanzania, three in China, two in Canada, two in Korea, two in Bolivia, two in UK, two in Belgium, one in each of the Vietnam, Egypt, Iran, Taiwan, Bangladesh, South Africa, India, Indonesia, Mexico, and Agra. Table 3 provides more details about the final included articles.

3.1. LABs and Antiviral Effects

L. rhamnosus GG and L. casei were the most LAB probiotics investigated in the literature. While most of the articles confirmed the antiviral effects of LABs, some evidence did not support this idea. Table 4 summarizes the antiviral effects of LABs, including the present application, their effects on viral load/shedding, clinical outcomes, and laboratory modifications are attributable to LABS (Table 4). The antiviral mechanism proposed in the studies was summarized into three major categories: (1) direct effect of LAB on viruses (the most common mechanism), (2) production of antiviral compounds, and (3) stimulation of the immune system against viruses. These mechanisms are discussed in more detail subsequently.

Another notable aspect of our study is the antiviral effects of LABs in immunocompromised patients. While most of the postulated mechanisms have been about immunocompetent individuals, studies in immunocompromised patients, such as HIV+ patients, dedicate activation of immune cells such as CD4+ cells, amelioration of inflammation, and decrease in translocation markers. The attributable mechanisms would be explained subsequently.

4. Discussion

As we have stated so far, five of the selected 45 publications revealed no discernible impact on the viruses. These five articles were administered L. rhamnosus; two had L. helveticus, and one had B. animalis spp., Lactis in their administered probiotics in addition. The major explanation of this discrepancy could be the limited research population, the pathogen change, the comparison to vaccination, the varied study techniques from earlier studies, and the various months of patient enrollment in the study. According to the current evidence, central mechanisms of LAB antiviral effects can be categorized into three major groups: (1) the direct interactions between LABs and viruses, (2) the production of bioactive antiviral agents, and (3) the induction of interferon-associated mechanisms. We have summarized these mechanisms in Figure 2 and discuss each mechanism in more detail.(1)The direct interactions between LABs and viruses Direct interactions between the LABs and viruses are the primary mechanism of virus inactivation. The direct antiviral effect of LAB is applied via both adsorption and trapping, which are strain-dependent mechanisms and can inhibit viruses in a nonspecific and perhaps specific manner [5, 61]. Botić et al. showed that L. paracasei, L. rhamnosus, L. plantarum, and L. reuteri could trap vesicular stomatitis virus (VSV) [61]. Also, L. gasseri has direct antiviral ability against simplex type 2 (HSV-2) [62]. Some Lactobacillus strains can trap HIV virions by binding their glycoprotein gp120 to the mannose sugar-rich “dome” at the end of the HIV attachment proteins. These results suggest the existence of identical mechanisms in inhibiting viruses by LAB strains [63]. Notably, attaching LABs to the cell surface leads to blocking the binding of viruses to their receptors on the cell surface, preventing viruses from entering the cell in the early stages of infection [64, 65].(2)The production of bioactive antiviral agents Hydrogen peroxide (H₂O₂) and lactic acid produced by Lactobacillus spp. are two critical antimicrobial products of LAB. Both have antiviral effects against HIV-1 and HSV-2 via acidifying the pH of their microenvironment [66–69]. Bacteriocins are other groups of LAB products that play essential roles in destroying virus-infected cells via diverse mechanisms, such as creating holes in target cell membranes, lowering intracellular pH, and blocking enzymatic activities [70]. It is shown that L. delbruecki developed a noncytotoxic bacteriocin that was found to be virucidal against the influenza virus [71]. Exopolysaccharides (EPS) derived from the genus Leuconostoc spp. have shown antiviral activities against HSV-1 [72]. The EPS applies strong virucidal action and reduces the viral adsorption, penetration, and production of virus particles by 97–99%; EPSs 2t and 19s decrease viral progeny infectivity by blocking viral adsorption to cells [73]. EPS 26a is another family member with proven inhibitory effects on Human Adenovirus Type 5 (HAdV-5) reproduction [74]. EPS 26a has strong anti-HAdV-5 action by developing noninfectious viral offspring [74]. Other bacterial components, such as a non-protein-composed wall component, inhibit viral reproduction [75]. In cell cultures, a nonprotein cell wall component isolated from a vaginal strain of L. brevis significantly inhibited HSV-2 replication [75].(3)Induction of interferon-associated mechanisms LABs stimulate immune system components via lipopolysaccharide (LPS), lipoproteins, lipopeptides, and unmethylated CpG motifs mainly through toll-like receptors [76, 77].

Figure 2

A summary of the mechanisms of the antiviral effects of LABs. The first process involves interactions between LABs and viruses that trap or adhere viruses to the surface of the host cell, preventing them from adhering to cells. The generation of bioactive antiviral substances such as H2O2, lactic acid, bacteriocins, exopolysaccharides, etc., is the second mechanism. The third mechanism involves interferon-associated mechanisms, which include (a) activation of dendritic cells, which results in T-cell activation, production of cytokines, and inhibition of viral replication; (b) activation of the JAK-STAT signaling cascade, which results in transcription of genes with antiviral and immunomodulatory effects, as well as binding of ISG15 to viral proteins, which causes them to be destroyed; and (c) binding of bioactive substances to the toll-like receptor.

Moreover, M cells ingest LABs, producing interferon type I (type I IFN), which activates dendritic cells [78]. Activated dendritic cells trigger multiple critical intracellular signaling pathways, resulting in T-cell activation, viral replication inhibition, and production of immunomodulatory cytokines [79].

Production and secretion of IFNs provide a high level of antiviral protection [80]. The Janus kinase-Sign Transducer and Activator of Transcription (JAK-STAT) signaling cascade is activated by type I and type III IFNs, which phosphorylate STAT1 and STAT2 [81]. Phosphorylated STATs and the IFN Regulatory Factor-9 (IRF9) form the IFN-Stimulated Gene Factor 3 (ISGF3) complex [80]. The ISGF3 complex enters the cell nucleus and enhances the transcription of genes that have IFN-Stimulated Response Element (ISRE) in their promoters [80]. These genes might have antiviral or modulatory effects on the inflammation and cytokine production pathways [80]. Type II IFNs also cause STAT1 homodimerization, which favors ISG promoters with gamma-activated sequence (GAS) containing promoters [80]. All result in the induction and activation of several antiviral agents, including the protein kinase RNA-activated (PKR), ribonuclease 2-5A pathway, and numerous apoptotic pathways which inhibit the virus binding to cells, viral particle penetration into cells, and the release of the nucleocapsid from an envelope [82]. Disruption of transcription and translation processes of the structural viral proteins prevents virion formation or budding of viruses [83].

Another key mediator of IFN antiviral effects is interferon-stimulated gene 15 (ISG15), a ubiquitin-like protein that plays a significant role in counteracting viruses by conjugating to the viral and cellular proteins and marking them for destruction [84]. Three enzymes mediate the ISG15 conjugation with the target protein; E1 activating enzyme (Ube1L), E2 conjugating enzyme (UbcH8), and E3 ligase enzyme (either HERC5, or EFP, or TRIM25). These enzymes establish a covalent bond between the C-terminal glycine of the mature form of ISG15 and the target protein lysine [84–86]. Conjugation of ISG15 with viral proteins leads to impaired protein function, promotes protein degradation, and prevents oligomerization of viral proteins [87]. IFNs increase the poly-SUMOylation and ISGylation of both viral and cellular proteins [88]. As well, the ISG15 can modify and inhibit the viral mRNA translation by strengthening the attachment of translation suppressor proteins such as eIF4E homologous protein (4EHP) to the viral mRNA cap [89]. ISG15 is also secreted from various cells [90]. The extracellular ISG15 can also act as an antiviral cytokine by producing and secreting antiviral factors such as type III IFNs, nitric oxide (NO), and reactive oxygen species (ROS), which induce apoptosis in virus-infected cells [87, 91, 92]. Binding ISG15 to the lymphocyte function-associated antigen 1 (LFA-1), located on immune cells, results in cell proliferation, maturation, and production of IFN-γ and IL-10 [93–97]. Bioactive agents and LAB particles are essential ligands for toll-like receptors (TLRs) [98]. TLRs’ activation results in T-cell activation and cytokine production via mitogen-activated protein (MAP) kinases and NF-kB signaling pathways in dendritic cells [99]. MAP kinases directly phosphorylate the transcription factor AP-1, a key player in T-cell activation [100–102]. The phosphorylated AP-1 heterodimerizes in the nucleus and binds to the IL-2 promoter and enhance its expression which promotes the T-cell activity [102].

5. Conclusion

According to the current literature, LABs have considerable antiviral activities which affect viruses both directly and indirectly. Although our study provides an overview of the antiviral activities of the LABs as one of the most important human gut microbiota, it has some limitations: the applicability of using LABs as antiviral adjuvants in clinical practice has not been fully investigated, and so it is not justifiable by our study. As well, the potential adverse effects of the therapeutic use of LABs and their delivery system as a therapeutic agent are not investigated. We propose further studies to investigate these concerns and promote our knowledge about more efficient antiviral agents.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon reasonable request.

Disclosure

A preprint has previously been published. The authors Fargol Farahmnandi and Parynaz Parhizgar are co-first authors. Our study is also aligned with these goals. In our comprehensive study, we concluded all available high-quality clinical studies that investigated the effectiveness and safety of lactic acid bacteria in viral infections. Our study is among limited evidence which systematically reviews the current application of lactic acid bacteria in viral diseases and provides a detailed concept of the attributable mechanisms which have not been previously investigated on this level. We confirm that this work is original and has not been published elsewhere, nor is it currently under consideration for publication elsewhere.

Conflicts of Interest

The authors declare that there are no conflicts of interest.

Authors’ Contributions

All authors contributed to the study conception and design. Literature search and data collection were performed by Fargol Farahmnandi, Parynaz Parhizgar, Fahimeh Bizhannia, Maede Hosseinzade, and Parya Mozafari Komesh Tape. The first draft of the manuscript was written by Fateme sadat rohani, Marzieh Bizhanzadeh, Zeinab Sadat Mostafavi Alhosseini, Maede Hosseinzade, Mohammad Javad Nasiri, and Yeganeh Farsi, and all the authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

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