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Probiotics and the Immune System: The Potential for Postimmunobiotics

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Gut Microbiota".

Deadline for manuscript submissions: closed (31 July 2023) | Viewed by 32261

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Special Issue Editors

Prof. Dr. Haruki Kitazawa

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Guest Editor

International Education and Research Center for Food and Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Aobaku, Sendai 980-8572, Japan
Interests: probiotics; immunobiotics; food immunology; feed immunology; mucosal immunology; inflammation
Special Issues, Collections and Topics in MDPI journals

Dr. Julio Villena

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Guest Editor

Laboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Chacabuco 145, San Miguel de Tucuman CP400, Argentina
Interests: probiotics; immunobiotics; mucosal immunology; genomics; lactic acid bacteria; microbiota
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. A. K. M. Humayun Kober

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Guest Editor

Chittagong Veterinary and Animal Sciences University, Bangladesh and JSPS Invitational Research Fellow, Lab. of Animal Food Function, Tohoku University, Sendai 980-8572, Japan
Interests: food microbiology; animal production; antimicrobial; immunobiotics; probiotics; functional foods
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Welcome to the Special Issue “Probiotics and the immune system: the potential for postimmunobiotics” of Microorganisms. Probiotic microorganisms are considered to support the host's health. Despite enlightening advances in research and development, validation of the health-promoting properties of probiotic products is still required, especially by regulators. Scientific criticism based on poorly characterized isolates, soft clinical targets, and the absence of a mechanistic framework limited the value of the probiotic concept. Thus, studies on how probiotics work at the cellular and molecular level are mandatory to expand their industrial applications.

The term 'immunobiotics' has been proposed to describe microbes able to beneficially modulate the host immune system. In recent years, reports have described the benefits of immunobiotics in mucosal and non-mucosal infections, allergies, inflammatory bowel disease, obesity, immunosuppression, antimicrobial substitutes, and other immune-mediated diseases. Bioactive compounds with immunomodulatory properties derived from immunobiotic microbes (postimmunobiotics) are being actively characterized by the scientific community. Research in postimmunobiotics applications may lead to the development of pharmabiotics that improve human or animal health through the modulation of the immune system. Immunobiotics and postimmunobiotics research has the potential to benefit the food, medical, and pharmaceutical industries.

As the Guest Editors of this Special Issue, we invite the submission of research articles, review articles, and short communications on the use of immunobiotics and postimmunobiotics to prevent or treat diseases and improve the health of human and animals.

This Special Issue welcomes contributions in this field covering the following areas:

Isolation and identification of novel immunobiotics;
Identification and characterization of novel postimmunobiotics;
Design and characterization of immunobiotics- or postimmunobiotics-supplemented functional products;
Effects of immunobiotics and postimmunobiotics products in the modulation of the microbiota;
Cellular and molecular interactions of immunobiotics and postimmunobiotics with the host;

We hope you will enjoy this issue.

Prof. Dr. Haruki Kitazawa
Dr. Julio Villena
Prof. Dr. A. K. M. Humayun Kober
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Microorganisms is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

probiotics
immunobiotics
postimmunobiotics
immunomodulation

Published Papers (9 papers)

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Research

Jump to: Review

13 pages, 2741 KiB

Open AccessArticle

Oral Administration of Lacticaseibacillus rhamnosus CRL1505 Modulates Lung Innate Immune Response against Klebsiella pneumoniae ST25

by Stefania Dentice Maidana, Yoshiya Imamura, Mariano Elean, Leonardo Albarracín, Keita Nishiyama, Yoshihito Suda, Shoichiro Kurata, María Ángela Jure, Haruki Kitazawa and Julio Villena

Microorganisms 2023, 11(5), 1148; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11051148 - 28 Apr 2023

Cited by 1 | Viewed by 1423

Abstract

Orally administered Lacticaseibacillus rhamnosus CRL1505 enhances respiratory immunity, providing protection against respiratory viruses and Streptococcus pneumoniae. However, the capacity of the CRL1505 strain to improve respiratory immunity against Gram-negative bacterial infections has not been evaluated before. The aim of this work was to evaluate whether the Lcb. rhamnosus CRL1505 was able to beneficially regulate the respiratory innate immune response and enhance the resistance to hypermucoviscous KPC-2-producing Klebsiella pneumoniae of the sequence type 25 (ST25). BALB/c mice were treated with the CRL1505 strain via the oral route and then nasally challenged with K. pneumoniae ST25 strains LABACER 01 or LABACER 27. Bacterial cell counts, lung injuries and the respiratory and systemic innate immune responses were evaluated after the bacterial infection. The results showed that K. pneumoniae ST25 strains increased the levels of TNF-α, IL-1β, IL-6, IFN-γ, IL-17, KC and MPC-1 in the respiratory tract and blood, as well as the numbers of BAL neutrophils and macrophages. Mice treated with Lcb. rhamnosus CRL1505 had significantly lower K. pneumoniae counts in their lungs, as well as reduced levels of inflammatory cells, cytokines and chemokines in the respiratory tract and blood when compared to infected controls. Furthermore, higher levels of the regulatory cytokines IL-10 and IL-27 were found in the respiratory tract and blood of CRL1505-treated mice than controls. These results suggest that the ability of Lcb. rhamnosus CRL1505 to help with the control of detrimental inflammation in lungs during K. pneumoniae infection would be a key feature to improve the resistance to this pathogen. Although further mechanistic studies are necessary, Lcb. rhamnosus CRL1505 can be proposed as a candidate to improve patients’ protection against hypermucoviscous KPC-2-producing strains belonging to the ST25, which is endemic in the hospitals of our region. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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22 pages, 4130 KiB

Open AccessArticle

Immunomodulatory and Antioxidant Properties of a Novel Potential Probiotic Bacillus clausii CSI08

by Ekaterina Khokhlova, Joan Colom, Annie Simon, Shahneela Mazhar, Guillermo García-Lainez, Silvia Llopis, Nuria Gonzalez, María Enrique-López, Beatriz Álvarez, Patricia Martorell, Marta Tortajada, John Deaton and Kieran Rea

Microorganisms 2023, 11(2), 240; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11020240 - 18 Jan 2023

Cited by 4 | Viewed by 4812

Abstract

Spore-forming bacteria of the Bacillus genus have demonstrated potential as probiotics for human use. Bacillus clausii have been recognized as efficacious and safe agents for preventing and treating diarrhea in children and adults, with pronounced immunomodulatory properties during several in vitro and clinical studies. Herein, we characterize the novel strain of B. clausii CSI08 (Munispore^®) for probiotic attributes including resistance to gastric acid and bile salts, the ability to suppress the growth of human pathogens, the capacity to assimilate wide range of carbohydrates and to produce potentially beneficial enzymes. Both spores and vegetative cells of this strain were able to adhere to a mucous-producing intestinal cell line and to attenuate the LPS- and Poly I:C-triggered pro-inflammatory cytokine gene expression in HT-29 intestinal cell line. Vegetative cells of B. clausii CSI08 were also able to elicit a robust immune response in U937-derived macrophages. Furthermore, B. clausii CSI08 demonstrated cytoprotective effects in in vitro cell culture and in vivo C. elegans models of oxidative stress. Taken together, these beneficial properties provide strong evidence for B. clausii CSI08 as a promising potential probiotic. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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16 pages, 2878 KiB

Open AccessArticle

Inferring Bacterial Community Interactions and Functionalities Associated with Osteopenia and Osteoporosis in Taiwanese Postmenopausal Women

by Yi-Jie Kuo, Chia-Jung Chen, Bashir Hussain, Hsin-Chi Tsai, Gwo-Jong Hsu, Jung-Sheng Chen, Aslia Asif, Cheng-Wei Fan and Bing-Mu Hsu

Microorganisms 2023, 11(2), 234; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11020234 - 17 Jan 2023

Cited by 1 | Viewed by 1656

Abstract

Growing evidence suggests that the gut microbiota and their metabolites are associated with bone homeostasis and fragility. However, this association is limited to microbial taxonomic differences. This study aimed to explore whether gut bacterial community associations, composition, and functions are associated with osteopenia and osteoporosis. We compared the gut bacterial community composition and interactions of healthy postmenopausal women with normal bone density (n = 8) with those of postmenopausal women with osteopenia (n = 18) and osteoporosis (n = 21) through 16S rRNA sequencing coupled with network biology and statistical analyses. The results of this study showed reduced alpha diversity in patients with osteoporosis, followed by that in patients with osteopenia, then in healthy controls. Taxonomic analysis revealed that significantly enriched bacterial genera with higher abundance was observed in patients with osteoporosis and osteopenia than in healthy subjects. Additionally, a co-occurrence network revealed that, compared to healthy controls, bacterial interactions were higher in patients with osteoporosis, followed by those with osteopenia. Further, NetShift analysis showed that a higher number of bacteria drove changes in the microbial community structure of patients with osteoporosis than osteopenia. Correlation analysis revealed that most of these driver bacteria had a significant positive relationship with several significant metabolic pathways. Further, ordination analysis revealed that height and T-score were the primary variables influencing the gut microbial community structure. Taken together, this study evaluated that microbial community interaction is more important than the taxonomic differences in knowing the critical role of gut microbiota in postmenopausal women associated with osteopenia and osteoporosis. Additionally, the significantly enriched bacteria and functional pathways might be potential biomarkers for the prognosis and treatment of postmenopausal women with osteopenia and osteoporosis. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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17 pages, 3180 KiB

Open AccessArticle

Lactiplantibacillus plantarum Strains Modulate Intestinal Innate Immune Response and Increase Resistance to Enterotoxigenic Escherichia coli Infection

by Ayelen Baillo, Julio Villena, Leonardo Albarracín, Mikado Tomokiyo, Mariano Elean, Kohtaro Fukuyama, Sandra Quilodrán-Vega, Silvina Fadda and Haruki Kitazawa

Microorganisms 2023, 11(1), 63; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11010063 - 25 Dec 2022

Cited by 3 | Viewed by 1807

Abstract

Currently, probiotic bacteria with not transferable antibiotic resistance represent a sustainable strategy for the treatment and prevention of enterotoxigenic Escherichia coli (ETEC) in farm animals. Lactiplantibacillus plantarum is among the most versatile species used in the food industry, either as starter cultures or probiotics. In the present work, the immunobiotic potential of L. plantarum CRL681 and CRL1506 was studied to evaluate their capability to improve the resistance to ETEC infection. In vitro studies using porcine intestinal epithelial (PIE) cells and in vivo experiments in mice were undertaken. Expression analysis indicated that both strains were able to trigger IL-6 and IL-8 expression in PIE cells in steady-state conditions. Furthermore, mice orally treated with these strains had significantly improved levels of IFN-γ and TNF-α in the intestine as well as enhanced activity of peritoneal macrophages. The ability of CRL681 and CRL1506 to beneficially modulate intestinal immunity was further evidenced in ETEC-challenge experiments. In vitro, the CRL1506 and CRL681 strains modulated the expression of inflammatory cytokines (IL-6) and chemokines (IL-8, CCL2, CXCL5 and CXCL9) in ETEC-stimulated PIE cells. In vivo experiments demonstrated the ability of both strains to beneficially regulate the immune response against this pathogen. Moreover, the oral treatment of mice with lactic acid bacteria (LAB) strains significantly reduced ETEC counts in jejunum and ileum and prevented the spread of the pathogen to the spleen and liver. Additionally, LAB treated-mice had improved levels of intestinal IL-10 both at steady state and after the challenge with ETEC. The protective effect against ETEC infection was not observed for the non-immunomodulatory TL2677 strain. Furthermore, the study showed that L. plantarum CRL1506 was more efficient than the CRL681 strain to modulate mucosal immunity highlighting the strain specific character of this probiotic activity. Our results suggest that the improved intestinal epithelial defenses and innate immunity induced by L. plantarum CRL1506 and CRL681 would increase the clearance of ETEC and at the same time, protect the host against detrimental inflammation. These constitute valuable features for future probiotic products able to improve the resistance to ETEC infection. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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22 pages, 3252 KiB

Open AccessArticle

The Ability of Postimmunobiotics from L. rhamnosus CRL1505 to Protect against Respiratory Syncytial Virus and Pneumococcal Super-Infection Is a Strain-Dependent Characteristic

by Fernanda Raya Tonetti, Patricia Clua, Kohtaro Fukuyama, Guillermo Marcial, Jacinto Sacur, Gabriela Marranzino, Mikado Tomokiyo, Guadalupe Vizoso-Pinto, Apolinaria Garcia-Cancino, Shoichiro Kurata, Haruki Kitazawa and Julio Villena

Microorganisms 2022, 10(11), 2185; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10112185 - 03 Nov 2022

Cited by 5 | Viewed by 1740

Abstract

Previously, we demonstrated that the non-viable strain Lacticaseibacillus rhamnosus CRL1505 (NV1505) or its purified peptidoglycan (PG1505) differentially modulated the respiratory innate antiviral immune response triggered by Toll-like receptor (TLR)-3 activation in infant mice, improving the resistance to primary respiratory syncytial virus (RSV) infection and secondary pneumococcal pneumonia. In this work, we evaluated the effect of other non-viable L. rhamnosus strains and their peptidoglycans on the respiratory immune response and their impact on primary and secondary respiratory infections. In addition, the duration of the protective effect induced by NV1505 and PG1505 as well as their ability to protect against different Streptococcus pneumoniae serotypes were evaluated. Our results showed that among the five selected L. rhamnosus strains (CRL1505, CRL498, CRL576, UCO25A and IBL027), NV1505 and NVIBL027 improved the protection against viral and pneumococcal infections by modulating the respiratory immune response. Of note, only the PG1505 presented immunomodulatory activities when compared with the other purified peptidoglycans. Studies on alveolar macrophages showed that NV1505 and PG1505 differentially modulated the expression of IL-6, IFN-γ, IFN-β, TNF-α, OAS1, RNAseL and IL-27 genes in response to RSV infection, and IL-6, IFN-γ, IL-1β, TNF-α, CCL2, CXCL2, CXCL10 and IL-27 in response to pneumococcal challenge. Furthermore, we demonstrated that NV1505 and PG1505 treatments protected mice against secondary pneumococcal pneumonia produced by different serotypes of S. pneumoniae until 30 days after stimulation with poly(I:C). This work advances the characterization of the protective effect of NV1505 and PG1505 by demonstrating that they increase resistance against the pneumococcal serotypes 3, 6B, 14 and 19F, with an effect that lasts up to 30 days after the primary viral inflammation. The results also confirm that the immunomodulatory properties of NV1505 and PG1505 are unique and are not shared by other members of this species, and suggest the existence of a capacity to stimulate trained immunity in alveolar macrophages. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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13 pages, 2575 KiB

Open AccessArticle

Lactobacillus paragasseri BBM171 Ameliorates Allergic Airway Inflammation Induced by Ovalbumin in Mice via Modulating the Th1/Th2 Balance

by Shih-Hsuan Cheng, Tzu-Ying Yang, Chih-Chieh Hsu, Yu-Hsuan Wei, Chien-Chen Wu and Ying-Chieh Tsai

Microorganisms 2022, 10(10), 2041; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10102041 - 15 Oct 2022

Cited by 6 | Viewed by 1701

Abstract

Supplementation with specific probiotics has been shown to improve allergic airway symptoms. This study aimed to investigate immunomodulatory effects of a potential probiotic strain isolated from breast milk, Lactobacillus paragasseri BBM171 (BBM171), in an ovalbumin (OVA)-induced allergic mouse model. OVA-sensitized and OVA-challenged BALB/c mice were orally administered live or heat-inactivated BBM171 for 48 consecutive days. After the last allergen challenge, serum immunoglobulin (Ig) levels, inflammatory cell levels in the lungs, and cytokine levels in bronchoalveolar lavage fluid (BALF) were assessed. The results showed that oral administration of live or heat-inactivated BBM171 decreased serum levels of total IgE, OVA-specific IgE, and OVA-specific IgG1, while increasing OVA-specific IgG2a and reducing the extent of airway inflammation in OVA-induced allergic mice. In addition, both live and heat-inactivated BBM171 modulated the cytokine profile in BALF to a type 1 T helper (Th1) response. Furthermore, ex vivo experiments using OVA-induced allergic mouse splenocytes showed that both live and heat-inactivated BBM171 could regulate the Th1/Th2 balance, decrease the proinflammatory cytokine interleukin (IL)-17 level, and increase the anti-inflammatory cytokine IL-10 level. Taken together, these results suggest that oral administration of live or heat-inactivated BBM171 improved allergen-induced airway inflammation symptoms by modulating the host immune response toward Th1 dominance. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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Review

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14 pages, 1134 KiB

Open AccessReview

Lactobacilli and Their Probiotic Effects in the Vagina of Reproductive Age Women

by Sonal Pendharkar, Axel Skafte-Holm, Gizem Simsek and Thor Haahr

Microorganisms 2023, 11(3), 636; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11030636 - 01 Mar 2023

Cited by 3 | Viewed by 9875

Abstract

In the present narrative review, the probiotic effects of vaginal Lactobacillus spp. are described in detail, covering the importance of the differential production of lactic acid, the lactic acid D/L isoforms, the questionable in vivo effect of hydrogen peroxide, as well as bacteriocins and other core proteins produced by vaginal Lactobacillus spp. Moreover, the microbe–host interaction is explained with emphasis on the vaginal mucosa. To understand the crucial role of Lactobacillus spp. dominance in the vaginal microbiota, different dysbiotic states of the vagina are explained including bacterial vaginosis and aerobic vaginitis. Finally, this review takes on the therapeutic aspect of live lactobacilli in the context of bacterial vaginosis. Until recently, there was very low-quality evidence to suggest that any probiotic might aid in reducing vaginal infections or dysbiosis. Therefore, clinical usage or over the counter usage of probiotics was not recommended. However, recent progress has been made, moving from probiotics that are typically regulated as food supplements to so-called live biotherapeutic products that are regulated as medical drugs. Thus, recently, a phase 2b trial using a Lactobacillus crispatus strain as a therapeutic add-on to standard metronidazole showed significant reduction in the recurrence of bacterial vaginosis by 12 weeks compared to placebo. This may constitute evidence for a brighter future where the therapeutic use of lactobacilli can be harnessed to improve women’s health. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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18 pages, 2659 KiB

Open AccessReview

Probiotics and Postbiotics as the Functional Food Components Affecting the Immune Response

by Aleksandra Szydłowska and Barbara Sionek

Microorganisms 2023, 11(1), 104; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11010104 - 31 Dec 2022

Cited by 13 | Viewed by 4384

Abstract

The food market is one of the most innovative segments of the world economy. Recently, among consumers there is a forming trend of a healthier lifestyle and interest in functional foods. Products with positive health properties are a good source of nutrients for consumers’ nutritional needs and reduce the risk of metabolic diseases such as diabetes, atherosclerosis, or obesity. They also seem to boost the immune system. One of the types of functional food is “probiotic products”, which contain viable microorganisms with beneficial health properties. However, due to some technical difficulties in their development and marketing, a new alternative has started to be sought. Many scientific studies also point to the possibility of positive effects on human health, the so-called “postbiotics”, the characteristic metabolites of the microbiome. Both immunobiotics and post-immunobiotics are the food components that affect the immune response in two ways: as inhibition (suppressing allergies and inflammation) or as an enhancement (providing host defenses against infection). This work’s aim was to conduct a literature review of the possibilities of using probiotics and postbiotics as the functional food components affecting the immune response, with an emphasis on the most recently published works. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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20 pages, 1164 KiB

Open AccessReview

Probiotics in Periodontal and Peri-Implant Health Management: Biofilm Control, Dysbiosis Reversal, and Host Modulation

by Massimo Amato, Federica Di Spirito, Francesco D’Ambrosio, Giovanni Boccia, Giuseppina Moccia and Francesco De Caro

Microorganisms 2022, 10(11), 2289; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10112289 - 18 Nov 2022

Cited by 25 | Viewed by 3224

Abstract

Periodontitis and peri-implantitis are microbially associated diseases of the tissues supporting the teeth and dental implants that are mediated by host inflammation and eventually lead to tooth and dental implant loss. Given the probiotics’ role in biofilm control, dysbiosis reversal, and host modulation, their potential beneficial effects on the improvement of periodontitis and peri-implantitis have been recently investigated. Moreover, probiotics use has also been proposed in periodontal health management in patients undergoing fixed orthodontic therapy. Therefore, the present study aimed to review, considering the periodontal microbiome composition around teeth and dental implants in healthy and pathological conditions, the putative favorable effects of probiotics on gingivitis, periodontitis, and peri-implantitis. The secondary aim of the present narrative review was to synthesize the supporting evidence and proposed protocols for probiotics use as adjuncts in periodontitis and peri-implantitis treatment and the periodontal health management of orthodontic patients with fixed appliances. Contrasting findings from the literature may be due to the different methods, posology, and duration of probiotics prescriptions and due to the heterogeneous biological and clinical measurement methods employed. Thus, no definitive conclusions could be drawn about the effectiveness of probiotics in periodontal management, both in healthy and pathological conditions. Further studies are needed to validate probiotics for periodontal management and provide recommended protocols. Full article

(This article belongs to the Special Issue Probiotics and the Immune System: The Potential for Postimmunobiotics)

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