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Tüsüz Önata E, Özdemir Ö. Fecal microbiota transplantation in allergic diseases. World J Methodol 2025; 15:101430. [DOI: 10.5662/wjm.v15.i2.101430] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/13/2024] [Revised: 10/17/2024] [Accepted: 11/01/2024] [Indexed: 11/27/2024] Open
Abstract
Microorganisms such as bacteria, fungi, viruses, parasites living in the human intestine constitute the human intestinal microbiota. Dysbiosis refers to compositional and quantitative changes that negatively affect healthy gut microbiota. In recent years, with the demonstration that many diseases are associated with dysbiosis, treatment strategies targeting the correction of dysbiosis in the treatment of these diseases have begun to be investigated. Faecal microbiota transplantation (FMT) is the process of transferring faeces from a healthy donor to another recipient in order to restore the gut microbiota and provide a therapeutic benefit. FMT studies have gained popularity after probiotic, prebiotic, symbiotic studies in the treatment of dysbiosis and related diseases. FMT has emerged as a potential new therapy in the treatment of allergic diseases as it is associated with the maintenance of intestinal microbiota and immunological balance (T helper 1/T helper 2 cells) and thus suppression of allergic responses. In this article, the definition, application, safety and use of FMT in allergic diseases will be discussed with current data.
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Affiliation(s)
- Ece Tüsüz Önata
- Division of Pediatric Allergy and Immunology, Medical Faculty, Sakarya University, Adapazarı 54100, Sakarya, Türkiye
| | - Öner Özdemir
- Division of Pediatric Allergy and Immunology, Medical Faculty, Sakarya University, Adapazarı 54100, Sakarya, Türkiye
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Liu F, Zhang H, Fan L, Yu Q, Wang S. Hotspots and development trends of gut microbiota in atopic dermatitis: A bibliometric analysis from 1988 to 2024. Medicine (Baltimore) 2024; 103:e40931. [PMID: 39686442 PMCID: PMC11651439 DOI: 10.1097/md.0000000000040931] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/21/2024] [Accepted: 11/24/2024] [Indexed: 12/18/2024] Open
Abstract
BACKGROUND Atopic dermatitis (AD) is a prevalent inflammatory skin condition that commonly occurs in children. More and more scientific evidence suggests that gut microbiota plays an important role in the pathogenesis of AD, whereas there is no article providing a comprehensive summary and analysis. We aimed to analyze documents on AD and gut microbiota and identify hotspots and development trends in this field. METHODS Articles and reviews in the field of AD and gut microbiota from January 1, 1988 to October 20, 2024 were obtained from the Web of Science Core Collection database. Biblioshiny was utilized for evaluating and visualizing the core authors, journals, countries, documents, trend topics, and hotspots in this field. RESULTS Among 1672 documents, it indicated that the number of annual publications generally increased. The United States had the highest production, impact, and international collaboration. Journal of Allergy and Clinical Immunology was the journal of the maximum publications. Based on keyword co-occurrence and clustering analysis, "stratum-corneum lipids," "probiotics," "prebiotics," "fecal microbiota transplantation," "phage therapy," "short chain fatty-acids," "biologic therapy," and "skin inflammation" represented current trend topics. The pathological and molecular mechanisms and associated therapeutic methods for AD and gut microbiota were the research hotspots. The incorporation of microbiota-based therapies alongside conventional treatments can contribute to better clinical outcomes. CONCLUSION We highlighted that gut microbiota may exacerbate symptoms of AD through various aspects, including immunity, metabolites, and neuroendocrine pathways. More efforts are required to investigate the safety and efficacy of gut microbial management methods for the prevention and treatment of AD.
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Affiliation(s)
- Fang Liu
- Hangzhou Linping District Maternal and Child Health Care Hospital, Hangzhou, China
| | - Haipeng Zhang
- Hangzhou Linping District Maternal and Child Health Care Hospital, Hangzhou, China
| | - Lina Fan
- Hangzhou Linping District Maternal and Child Health Care Hospital, Hangzhou, China
| | - Qi Yu
- Chengdong College, Northeast Agricultural University, Harbin, China
| | - Siqiao Wang
- Tongji Hospital Affiliated to Tongji University School of Medicine, Shanghai, China
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Ramchandani R, Lucyshyn R, Linton S, Ellis AK. Breaking the mold: nontraditional approaches to allergen immunotherapy for environmental allergens. Immunotherapy 2024; 16:1153-1169. [PMID: 39382452 PMCID: PMC11633400 DOI: 10.1080/1750743x.2024.2408216] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/04/2024] [Accepted: 09/20/2024] [Indexed: 10/10/2024] Open
Abstract
Allergen immunotherapy is a disease-modifying treatment for allergic diseases. The predominant traditional immunotherapy is through subcutaneous administration of allergens to gradually desensitize allergic individuals. While effective, traditional allergen immunotherapy approaches are often lengthy, time consuming for patients and can result in local or systemic adverse reactions. Nontraditional immunotherapies are emerging as promising alternatives, offering potentially more convenient, safe and efficacious treatment options. This review sought to comprehensively examine the safety, efficacy and performance of various nontraditional immunotherapies for environmental allergens. Nontraditional immunotherapy approaches covered in this review include sublingual, local nasal, intralymphatic rush and ultra-rush immunotherapy, allergoid, microbial and anti-IgE immunotherapies. Nontraditional immunotherapies show significant promise in addressing the limitations of traditional subcutaneous immunotherapy. Methods like intralymphatic and rush immunotherapy offer shorter treatment regimens, enhancing patient adherence and convenience. The co-administration of probiotics or monoclonal antibodies, like omalizumab, with AIT appears to improve treatment efficacy and safety. Despite these advancements, further large-scale, long-term studies are needed to establish standardized protocols, dosing and validate long-term effects of these nontraditional immunotherapies. Standardizing outcome measurements across studies is crucial for accurate comparisons of nontraditional immunotherapies prior to widespread clinical adoption of these innovative techniques.
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Affiliation(s)
- Rashi Ramchandani
- Department of Medicine, University of Ottawa, Ottawa, ON, Canada
- Institute of Health Policy, Management & Evaluation, University of Toronto, Toronto, ON, Canada
| | - Rachel Lucyshyn
- Faculty of Health Sciences, Queen's University, Kingston, ON, Canada
- Allergy Research Unit, Kingston Health Sciences Center – KGH Site, Kingston, ON, Canada
| | - Sophia Linton
- Department of Medicine, Queen's University, Kingston, ON, Canada
- Department of Biomedical & Molecular Sciences, Queen's University, Kingston, Canada
| | - Anne K Ellis
- Allergy Research Unit, Kingston Health Sciences Center – KGH Site, Kingston, ON, Canada
- Department of Medicine, Queen's University, Kingston, ON, Canada
- Department of Biomedical & Molecular Sciences, Queen's University, Kingston, Canada
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Nagle S, Kumar P, kakde N. A Comparative Study to Assess the Add on Effects of Probiotic in Allergic Rhinitis Patients in a Tertiary Care Hospital. Indian J Otolaryngol Head Neck Surg 2023; 75:934-940. [PMID: 37206758 PMCID: PMC10188735 DOI: 10.1007/s12070-023-03481-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/06/2022] [Accepted: 01/09/2023] [Indexed: 02/02/2023] Open
Abstract
Probiotic intervention may have a promising role in the prevention of AR, in preventing allergic diseases including AR. Probiotics can exert beneficial effects on the host through distinct cellular and molecular pathways, these mechanisms of action may vary from one kind of probiotic to another for the same immune response and may be regulated by a combination of several events. Material and methods- Research site-Tertiary Care Government Hospital and Medical College in a major metropolitan city.TYPE OF STUDY-Prospective comparative Study.No. of Subjects -100 cases.Study Duration-Duration for collection of data-24 months.Sample size -100 patientsData Collection:Was collected from data of case proforma of all patients.Mode of Selection -Patients presenting in Out Patient Department (OPD)and In PatientDepartment(IPD) who meet the inclusion criteria and who consent to be a part of the study.Results-Significant difference was found in 12 weeks of treatment among group A and group B. Mild symptoms were seen more after 12 weeks in group B while severity of symptom reduction was less in group A as compared to group B in 12 weeks of treatment.Conclusion Probiotic intervention may have a promising role in the prevention of AR, in preventing allergic diseases including AR.Probiotics can exert beneficial effects on the host through distinct cellular and molecular pathways, these mechanisms of action may vary from one kind of probiotic to another for the same immune response and may be regulated by a combination of several events. Thus making probiotics' mechanism of action a challenging, complex, and fertile area for investigation. Probiotics appear to prevent allergy recurrences, alleviate the severity of symptoms and improve the quality of life of patients with allergic rhinitis.
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Affiliation(s)
- Smita Nagle
- Grant Government Medical College, Mumbai, 08 India
| | - Purnima Kumar
- Department of ENT, Grant Government Medical College, Mumbai, India
| | - Nilesh kakde
- Department of ENT, Grant Government Medical College, Mumbai, India
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The gut microbiome and allergic rhinitis; refocusing on the role of probiotics as a treatment option. Eur Arch Otorhinolaryngol 2023; 280:511-517. [PMID: 36239785 DOI: 10.1007/s00405-022-07694-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/24/2022] [Accepted: 10/05/2022] [Indexed: 01/21/2023]
Abstract
INTRODUCTION In the industrialized world, the incidence of Allergic rhinitis (AR), often known as hay fever, and other allergic disorders continues to grow. Recent studies have suggested environmental variables such as bacterial exposures as a potential reason for the rising prevalence of AR. With breakthroughs in our abilities to research the complex crosstalk of bacteria, the gut microbiomes' effect on human development, nutritional requirements, and immunologic disorders has become apparent METHODS: Three search engines, including Scopus, Medline, and PubMed, were searched for related published articles up to and including 1st July 2022. RESULTS Several studies have investigated links between commensal microbiome alterations and the development of atopic diseases such as asthma and AR. Besides, studies using probiotics for treating AR suggest that they may alleviate symptoms and improve patient's quality of life. CONCLUSION Research on probiotics and synbiotics for AR suggests they may improve symptoms, quality of life, and laboratory indicators. A better treatment strategy with advantages for patients may be achieved using probiotics, but only if more detailed in vitro and in vivo investigations are conducted with more participants.
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Galvan Calle CA, Díaz Vásquez C, Muñoz Leon R, Matos Benavides EE, Verde Leon AV. Clinical efficacy of synbiotics in children with allergic rhinitis: An observational cohort study from a private medical center in Peru. Immun Inflamm Dis 2022; 10:e736. [PMID: 36444623 PMCID: PMC9667200 DOI: 10.1002/iid3.736] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/29/2022] [Revised: 10/21/2022] [Accepted: 10/24/2022] [Indexed: 11/18/2022] Open
Abstract
BACKGROUND Probiotics in allergic rhinitis (AR) have shown improvement in clinical and quality of life scores, whereas the role of synbiotics in the treatment of AR has been poorly investigated. The purpose of this study was to evaluate the clinical efficacy of synbiotics in children with AR. METHODS An observational, prospective cohort study of pediatric outpatients with AR from a private medical center in Peru (2021) was conducted. At baseline, patients who were prescribed synbiotics during routine and those who were not (controls) recruited and followed up on Days 30, 60, and 90 of follow-up. Clinical efficacy was assessed with differences in Visual Analogous Scale (VAS), Total Nasal Symptom Score (TNSS), Rhinitis Control Assessment Test (RCAT), and the Pediatric Rhinoconjunctivitis Quality of Life Questionnaire (PRQLQ) scores between groups at follow-up. Mean differences ± standard deviation (SD) and 95% confidence intervals (95% CI) are reported. RESULTS Two hundred and fifteen participants were analyzed. Compared to controls (n = 115), those who used synbiotics (n = 100) had significantly lower VAS (mean difference 1.3; 95% CI: 0.8-1.8), TNSS (mean difference 1.1; 95% CI: 0.5-1.7) and higher RCAT scores and PRQLQ scores (mean difference 2.2; 95% CI: -3.3 to -1.2) and (mean difference 7.0; 95% CI: 3.1-10.9), respectively, at Day 90 of follow-up CONCLUSIONS: This paper reports significant improvement in clinical (VAS, RCAT, TNSS) and quality of life (PRQLQ) scores of small and large sizes, respectively. These preliminary findings support the need of future trials to assess the role of synbiotics in children with AR.
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Affiliation(s)
| | - Cecilia Díaz Vásquez
- Instituto Nacional de Salud del NiñoLimaPeru
- Instituto Nacional de Salud del Niño San BorjaLimaPeru
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Lu Y, Xing S, He L, Li C, Wang X, Zeng X, Dai Y. Characterization, High-Density Fermentation, and the Production of a Directed Vat Set Starter of Lactobacilli Used in the Food Industry: A Review. Foods 2022; 11:3063. [PMID: 36230139 PMCID: PMC9563398 DOI: 10.3390/foods11193063] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/16/2022] [Revised: 09/15/2022] [Accepted: 09/29/2022] [Indexed: 11/16/2022] Open
Abstract
Lactobacilli have been widely concerned for decades. Bacteria of the genus Lactobacillus have been commonly employed in fermented food to improve the appearance, smell, and taste of food or prolong its shelf-life. They comprise 261 species (by March 2020) that are highly diverse at the phenotypic, ecological, and genotypic levels. Some Lactobacilli strains have been documented to be essential probiotics, which are defined as a group of living microorganisms that are beneficial to the health of the host when ingested in sufficiency. However, the characterization, high-density fermentation, and the production of a directed vat set (DVS) starter of Lactobacilli strains used in the food industry have not been systematically reported. This paper mainly focuses on reviewing Lactobacilli as functional starter cultures in the food industry, including different molecular techniques for identification at the species and strain levels, methods for evaluating Lactobacilli properties, enhancing their performance and improving the cell density of Lactobacilli, and the production techniques of DVS starter of Lactobacilli strains. Moreover, this review further discussed the existing problems and future development prospects of Lactobacilli in the food industry. The viability and stability of Lactobacilli in the food industry and gastrointestinal environment are critical challenges at the industrial scale. The new production equipment and technology of DVS starter of Lactobacilli strains will have the potential for large-scale application, for example, developing low-temperature spray drying, freezing granulation drying, and spray freeze-drying.
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Affiliation(s)
- Yun Lu
- Key Laboratory of Agricultural and Animal Products Storage & Processing of Guizhou Province, Guizhou University, Guiyang 550025, China
- Department of Brewing Engineering, Moutai University, Renhuai 564507, China
| | - Shuqi Xing
- Key Laboratory of Agricultural and Animal Products Storage & Processing of Guizhou Province, Guizhou University, Guiyang 550025, China
- College of Liquor and Food Engineering, Guizhou University, Guiyang 550025, China
| | - Laping He
- Key Laboratory of Agricultural and Animal Products Storage & Processing of Guizhou Province, Guizhou University, Guiyang 550025, China
- College of Liquor and Food Engineering, Guizhou University, Guiyang 550025, China
| | - Cuiqin Li
- Key Laboratory of Agricultural and Animal Products Storage & Processing of Guizhou Province, Guizhou University, Guiyang 550025, China
- College of Liquor and Food Engineering, Guizhou University, Guiyang 550025, China
- School of Chemistry and Chemical Engineering, Guizhou University, Guiyang 550025, China
| | - Xiao Wang
- Key Laboratory of Agricultural and Animal Products Storage & Processing of Guizhou Province, Guizhou University, Guiyang 550025, China
- College of Liquor and Food Engineering, Guizhou University, Guiyang 550025, China
| | - Xuefeng Zeng
- Key Laboratory of Agricultural and Animal Products Storage & Processing of Guizhou Province, Guizhou University, Guiyang 550025, China
- College of Liquor and Food Engineering, Guizhou University, Guiyang 550025, China
| | - Yifeng Dai
- Key Laboratory of Agricultural and Animal Products Storage & Processing of Guizhou Province, Guizhou University, Guiyang 550025, China
- College of Liquor and Food Engineering, Guizhou University, Guiyang 550025, China
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Iftikhar H, Awan MO, Awan MS, Mustafa K, Das JK, Ahmed SK. Role of Probiotics in Patients with Allergic Rhinitis: A Systematic Review of Systematic Reviews. Int Arch Otorhinolaryngol 2022; 26:e744-e752. [PMID: 36405454 PMCID: PMC9668414 DOI: 10.1055/s-0042-1749370] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/30/2021] [Accepted: 04/17/2022] [Indexed: 10/18/2022] Open
Abstract
Introduction Allergic rhinitis (AR) is estimated to affect up to 30% of the world population. With the rise in cases, newer treatment modalities have been explored. Probiotics have shown to reduce symptoms of AR and improve quality of life. A few systematic reviews have been published aiming to assess the role of probiotics in AR. Objectives To consolidate the recent evidence with an overview of systematic reviews by extracting data regarding subjective outcomes (from quality of life questionnaires, the Total Nasal Symptom Score, the Total Ocular Symptom Score, the Daily Total Symptom Score, the incidence of AR, and the Rhinitis Total Symptom Score) and objective outcomes (levels of antigen-specific immunoglobulin E [IgE], total IgE, interleukin 10 [IL-10], interferon gamma [IFNG], eosinophil, and the T helper 1/T helper 2 [Th1/Th2] ratio). Data Synthesis We conducted a literature search on the PubMed, EBSCO CINAHL, EBSCO Dentistry & Oral Sciences Source, and Cochrane Library up to April 14, 2020. The qualitative assessment was performed using the Assessing the Methodological Quality of Systematic Reviews (AMSTAR-2) tool. A total of 419 titles were screened, and 3 systematic reviews met our eligibility criteria. Probiotics in the treatment of AR have been shown to improve quality of life, the total nasal and ocular symptom scores, the daily total symptom scores and Th1/Th2 ratio. No difference was ascertained for rhinitis total symptom score, and the rates of antigen-specific IgE, total IgE, IL-10, INFG and eosinophil. Conclusion The present review showed that there is considerable evidence that probiotics are useful in the treatment of AR. Further randomized trials targeting the limitations of the currently-available evidence can help ascertain the usefulness of probiotics in cases of AR.
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Affiliation(s)
- Haissan Iftikhar
- Department of Otolaryngology, Rawal Institute of Health Sciences, Islamabad, Pakistan
| | - Muhammad Ozair Awan
- Department of Surgery, Aga Khan University Medical College, Karachi, Pakistan
| | | | - Khawaja Mustafa
- Department of Surgery, Aga Khan University Medical College, Karachi, Pakistan
| | - Jai K. Das
- Division of Women and Child Health, Aga Khan University, Karachi, Pakistan
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Saeed NK, Al-Beltagi M, Bediwy AS, El-Sawaf Y, Toema O. Gut microbiota in various childhood disorders: Implication and indications. World J Gastroenterol 2022; 28:1875-1901. [PMID: 35664966 PMCID: PMC9150060 DOI: 10.3748/wjg.v28.i18.1875] [Citation(s) in RCA: 34] [Impact Index Per Article: 11.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/19/2022] [Revised: 03/08/2022] [Accepted: 03/27/2022] [Indexed: 02/06/2023] Open
Abstract
Gut microbiota has a significant role in gut development, maturation, and immune system differentiation. It exerts considerable effects on the child's physical and mental development. The gut microbiota composition and structure depend on many host and microbial factors. The host factors include age, genetic pool, general health, dietary factors, medication use, the intestine's pH, peristalsis, and transit time, mucus secretions, mucous immunoglobulin, and tissue oxidation-reduction potentials. The microbial factors include nutrient availability, bacterial cooperation or antagonism, and bacterial adhesion. Each part of the gut has its microbiota due to its specific characteristics. The gut microbiota interacts with different body parts, affecting the pathogenesis of many local and systemic diseases. Dysbiosis is a common finding in many childhood disorders such as autism, failure to thrive, nutritional disorders, coeliac disease, Necrotizing Enterocolitis, helicobacter pylori infection, functional gastrointestinal disorders of childhood, inflammatory bowel diseases, and many other gastrointestinal disorders. Dysbiosis is also observed in allergic conditions like atopic dermatitis, allergic rhinitis, and asthma. Dysbiosis can also impact the development and the progression of immune disorders and cardiac disorders, including heart failure. Probiotic supplements could provide some help in managing these disorders. However, we are still in need of more studies. In this narrative review, we will shed some light on the role of microbiota in the development and management of common childhood disorders.
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Affiliation(s)
- Nermin Kamal Saeed
- Medical Microbiology Section, Department of Pathology, Salmaniya Medical Complex, Ministry of Health, Manama 12, Bahrain
- Microbiology Section, Department of Pathology, Irish Royal College of Surgeon, Busaiteen 15503, Bahrain
| | - Mohammed Al-Beltagi
- Department of Pediatrics, University Medical Center, Arabian Gulf University, Dr. Sulaiman Al Habib Medical Group, Manama 26671, Bahrain
- Department of Pediatrics, Faculty of Medicine, Tanta University, Tanta 31511, Egypt
| | - Adel Salah Bediwy
- Department of Chest Disease, Faculty of Medicine, Tanta University, Tanta 31527, Egypt
- Department of Pulmonology, University Medical Center, Arabian Gulf University, Dr. Sulaiman Al Habib Medical Group, Manama 26671, Bahrain
| | - Yasser El-Sawaf
- Department of Tropical Medicine, Faculty of Medicine, Tanta University, Tanta 31527, Egypt
- Department of Gastroenterology, University Medical Center, Arabian Gulf University, Dr. Sulaiman Al-Habib Medical Group, Manama 26671, Bahrain
| | - Osama Toema
- Department of Pediatrics, Faculty of Medicine, Tanta University, Tanta 31511, Egypt
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Mårtensson A, Nordström F, Cervin-Hoberg C, Lindstedt M, Sakellariou C, Cervin A, Greiff L. Nasal administration of a probiotic assemblage in allergic rhinitis: a placebo-controlled crossover experimental study. Clin Exp Allergy 2022; 52:774-783. [PMID: 35075723 PMCID: PMC9314659 DOI: 10.1111/cea.14098] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/10/2021] [Revised: 01/03/2022] [Accepted: 01/14/2022] [Indexed: 11/27/2022]
Abstract
BACKGROUND Topical probiotics have been suggested as a treatment option for allergic rhinitis, as they may skew the immune response towards a beneficial type-1 non-allergic profile. So far observations in man have exclusively involved oral intake. The aim of this study was to examine if a topical/nasal administration of a probiotic assemblage (PA) affects quality of life, symptoms, and signs of allergic rhinitis in a nasal allergen challenge (NAC) model. METHODS In a placebo-controlled and crossover design, 24 patients with seasonal allergic rhinitis were subjected to topical/nasal administration with a PA of Lactobacillus rhamnosus SP1, Lactobacillus paracasei 101/37, and Lactococcus lactis L1A for three weeks. The last week of each treatment period was combined with a NAC-series. Efficacy variables were "Mini-Rhinoconjunctivitis Quality of Life Questionnaire" (Mini-RQLQ), "Total Nasal Symptom Score" (TNSS), "Peak Nasal Inspiratory Flow" (PNIF), and "Fractional Exhaled Nitric Oxide" (FeNO). In addition, to assess whether or not the PA produced any pro-inflammatory effect per se, soluble analytes were monitored in nasal lavage fluids. Finally, bacterial cultures, sampled using swabs from the middle nasal meatus, were assessed for presence of the PA by MALDI-TOF analysis. RESULTS Administration of the PA did not produce any nasal symptoms (cf. placebo). An innate response was discerned within the PA-run (cf. baseline), but no change in nasal lavage fluid levels of cytokines/mediators were observed cf. placebo except for IL-17/IL-17A (a minor increase in the PA run). Administration of the PA did neither affect Mini-RQLQ, TNSS, PNIF, nor FeNO. No evidence of persistent colonization was observed. CONCLUSION Topical/nasal administration of a PA comprising Lactobacillus rhamnosus SP1, Lactobacillus paracasei 101/37, Lactococcus lactis L1A, while likely evoking a minor innate immune response yet being safe, does not affect quality of life, symptoms, or signs of allergic rhinitis.
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Affiliation(s)
- Anders Mårtensson
- Department of ORL, Head and Neck Surgery, Helsingborg Hospital, Lund, Sweden.,Department of Clinical Sciences, Lund University, Lund, Sweden
| | - Franziska Nordström
- Department of Clinical Sciences, Lund University, Lund, Sweden.,Department of ORL, Head and Neck Surgery, Skåne University Hospital, Lund, Sweden
| | - Charlotte Cervin-Hoberg
- Department of Clinical Sciences, Lund University, Lund, Sweden.,Department of ORL, Head and Neck Surgery, Skåne University Hospital, Lund, Sweden
| | - Malin Lindstedt
- Department of Immunotechnology, Lund University, Lund, Sweden
| | | | - Anders Cervin
- Department of ORL, Royal Brisbane & Women's Hospital, University of Queensland Centre for Clinical Research, Brisbane, Australia
| | - Lennart Greiff
- Department of Clinical Sciences, Lund University, Lund, Sweden.,Department of ORL, Head and Neck Surgery, Skåne University Hospital, Lund, Sweden
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Tramper‐Stranders G, Ambrożej D, Arcolaci A, Atanaskovic‐Markovic M, Boccabella C, Bonini M, Karavelia A, Mingomataj E, O' Mahony L, Sokolowska M, Untersmayr E, Feleszko W. Dangerous liaisons: Bacteria, antimicrobial therapies, and allergic diseases. Allergy 2021; 76:3276-3291. [PMID: 34390006 DOI: 10.1111/all.15046] [Citation(s) in RCA: 12] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/17/2021] [Accepted: 07/31/2021] [Indexed: 12/15/2022]
Abstract
Microbiota composition and associated metabolic activities are essential for the education and development of a healthy immune system. Microbial dysbiosis, caused by risk factors such as diet, birth mode, or early infant antimicrobial therapy, is associated with the inception of allergic diseases. In turn, allergic diseases increase the risk for irrational use of antimicrobial therapy. Microbial therapies, such as probiotics, have been studied in the prevention and treatment of allergic diseases, but evidence remains limited due to studies with high heterogeneity, strain-dependent effectiveness, and variable outcome measures. In this review, we sketch the relation of microbiota with allergic diseases, the overuse and rationale for the use of antimicrobial agents in allergic diseases, and current knowledge concerning the use of bacterial products in allergic diseases. We urgently recommend 1) limiting antibiotic therapy in pregnancy and early childhood as a method contributing to the reduction of the allergy epidemic in children and 2) restricting antibiotic therapy in exacerbations and chronic treatment of allergic diseases, mainly concerning asthma and atopic dermatitis. Future research should be aimed at antibiotic stewardship implementation strategies and biomarker-guided therapy, discerning those patients that might benefit from antibiotic therapy.
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Affiliation(s)
- Gerdien Tramper‐Stranders
- Department of Pediatrics Franciscus Gasthuis & Vlietland Rotterdam the Netherlands
- Department of Neonatology Erasmus Medical CenterSophia Children's Hospital Rotterdam the Netherlands
| | - Dominika Ambrożej
- Department of Pediatric Pneumonology and Allergy Medical University of Warsaw Warsaw Poland
- Doctoral School Medical University of Warsaw Warsaw Poland
| | - Alessandra Arcolaci
- Immunology Unit University of Verona and General Hospital Borgo Roma Hospital Verona Italy
| | | | - Cristina Boccabella
- Department of Cardiovascular and Thoracic Sciences Università Cattolica del Sacro CuoreFondazione Policlinico Universitario A. Gemelli – IRCCS Rome Italy
| | - Matteo Bonini
- Department of Cardiovascular and Thoracic Sciences Università Cattolica del Sacro CuoreFondazione Policlinico Universitario A. Gemelli – IRCCS Rome Italy
- National Heart and Lung Institute (NHLI) Imperial College London London UK
| | - Aspasia Karavelia
- Department of Ear‐Nose‐Throat surgery General Hospital of Kozani Kozani Greece
| | - Ervin Mingomataj
- Department of Allergology & Clinical Immunology ‘Mother Theresa’ School of Medicine Tirana Albania
| | - Liam O' Mahony
- Departments of Medicine and Microbiology APC Microbiome IrelandNational University of Ireland Cork Ireland
| | - Milena Sokolowska
- Swiss Institute of Allergy and Asthma Research (SIAF) University of Zurich Zurich Switzerland
| | - Eva Untersmayr
- Institute of Pathophysiology and Allergy Research Center for Pathophysiology, Infectiology and Immunology Medical University of Vienna Vienna Austria
| | - Wojciech Feleszko
- Department of Pediatric Pneumonology and Allergy Medical University of Warsaw Warsaw Poland
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Depoorter L, Vandenplas Y. Probiotics in Pediatrics. A Review and Practical Guide. Nutrients 2021; 13:2176. [PMID: 34202742 PMCID: PMC8308463 DOI: 10.3390/nu13072176] [Citation(s) in RCA: 44] [Impact Index Per Article: 11.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/17/2021] [Revised: 06/17/2021] [Accepted: 06/21/2021] [Indexed: 02/07/2023] Open
Abstract
The potential benefit of the administration of probiotics in children has been studied in many settings globally. Probiotics products contain viable micro-organisms that confer a health benefit on the host. Beneficial effects of selected probiotic strains for the management or prevention of selected pediatric conditions have been demonstrated. The purpose of this paper is to provide an overview of current available evidence on the efficacy of specific probiotics in selected conditions to guide pediatricians in decision-making on the therapeutic or prophylactic use of probiotic strains in children. Evidence to support the use of certain probiotics in selected pediatric conditions is often available. In addition, the administration of probiotics is associated with a low risk of adverse events and is generally well tolerated. The best documented efficacy of certain probiotics is for treatment of infectious gastroenteritis, and prevention of antibiotic-associated, Clostridioides difficile-associated and nosocomial diarrhea. Unfortunately, due to study heterogeneity and in some cases high risk of bias in published studies, a broad consensus is lacking for specific probiotic strains, doses and treatment regimens for some pediatric indications. The current available evidence thus limits the systematic administration of probiotics. The most recent meta-analyses and reviews highlight the need for more well-designed, properly powered, strain-specific and dedicated-dose response studies.
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Affiliation(s)
| | - Yvan Vandenplas
- Vrije Universiteit Brussel (VUB), UZ Brussel, KidZ Health Castle, 1090 Brussels, Belgium;
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Treatment with a Probiotic Mixture Containing Bifidobacterium animalis Subsp. Lactis BB12 and Enterococcus faecium L3 for the Prevention of Allergic Rhinitis Symptoms in Children: A Randomized Controlled Trial. Nutrients 2021; 13:nu13041315. [PMID: 33923532 PMCID: PMC8073063 DOI: 10.3390/nu13041315] [Citation(s) in RCA: 21] [Impact Index Per Article: 5.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/06/2021] [Revised: 04/11/2021] [Accepted: 04/13/2021] [Indexed: 12/25/2022] Open
Abstract
Background: Probiotics may prevent the allergic response development due to their anti-inflammatory and immunomodulatory effects. The aim of this study is to determine if the prophylactic treatment with a mixture of Bifidobacterium animalis subsp. Lactis BB12 and Enterococcus faecium L3 would reduce symptoms and need for drug use in children with allergic rhinitis (AR). Methods: The study included 250 children aged from 6 to 17 years, affected by AR. Patients were randomly assigned to the intervention group (150) or to the placebo group (100). Patients in the intervention group, in addition to conventional therapy (local corticosteroids and/or oral antihistamines), were treated in the 3 months preceding the onset of symptoms related to the presence of the allergen to which the children were most sensitized, with a daily oral administration of a probiotic mixture containing the Bifidobacterium animalis subsp. Lactis BB12 DSM 15954 and the Enterococcus faecium L3 LMG P-27496 strain. We used Nasal Symptoms Score (NSS) to evaluate AR severity before and after the treatment with probiotics or placebo. Results: the patients in the intervention group had a significant reduction in their NSS after probiotic treatment (p-value = 2.2 × 10−10. Moreover, for the same group of patients, we obtained a significant reduction in the intake of pharmacological therapy. In particular, we obtained a reduction in the use of oral antihistamines (p-value = 2.2 × 10−16), local corticosteroids (p-value = 2.2 × 10−13), and of both drugs (p-value 1.5 × 10−15). Conclusions: When administered as a prophylactic treatment, a mixture of BB12 and L3 statistically decreased signs and symptoms of AR and reduced significantly the need of conventional therapy.
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Meirlaen L, Levy EI, Vandenplas Y. Prevention and Management with Pro-, Pre and Synbiotics in Children with Asthma and Allergic Rhinitis: A Narrative Review. Nutrients 2021; 13:934. [PMID: 33799367 PMCID: PMC7999316 DOI: 10.3390/nu13030934] [Citation(s) in RCA: 23] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/16/2021] [Revised: 03/04/2021] [Accepted: 03/11/2021] [Indexed: 02/06/2023] Open
Abstract
Allergic diseases including allergic rhinitis and asthma are increasing in the developing world, related to a westernizing lifestyle, while the prevalence is stable and decreasing in the industrialized world. This paper aims to answer the question if prevention and/or treatment of allergic rhinitis and asthma can be achieved by administrating pro-, pre- and/or synbiotics that might contribute to stabilizing the disturbed microbiome that influences the immune system through the gut-lung axis. We searched for relevant English articles in PubMed and Google Scholar. Articles interesting for the topic were selected using subject heading and key words. Interesting references in included articles were also considered. While there is substantial evidence from animal studies in well controlled conditions that selected probiotic strains may offer benefits in the prevention of wheezing and asthma, outcomes from clinical studies in infants (including as well pre- and postnatal administration) are disappointing. The latter may be related to the multiple confounding factors such as environment, strain selection and dosage, moment of administration and genetic background. There is little evidence to recommend administration of pro, pre- or synbiotics in the prevention of asthma and allergic rhinitis in children.
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Affiliation(s)
| | | | - Yvan Vandenplas
- KidZ Health Castle, UZ Brussel, Vrije Universiteit Brussel, 1090 Brussels, Belgium; (L.M.); (E.I.L.)
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Bourdillon AT, Edwards HA. Review of probiotic use in otolaryngology. Am J Otolaryngol 2021; 42:102883. [PMID: 33453564 DOI: 10.1016/j.amjoto.2020.102883] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/16/2020] [Accepted: 12/25/2020] [Indexed: 12/18/2022]
Abstract
OBJECTIVE Probiotics have garnered considerable attention as an intervention for various conditions common to otolaryngology. The purpose of this review is to evaluate the current literature to offer recommendations about the safety and efficacy of probiotic management in otolaryngologic conditions. STUDY DESIGN Narrative review. METHODS PubMed and Google Scholar were queried using pertinent keywords to retrieve relevant studies with particular focus in the recent 5 years. All abstracts were assessed and studies, reviews and meta-analyses achieving evaluation of probiotic therapies or characterization of microbiome changes were included for further review. Studies were categorized by condition or anatomic region across various subspecialties. Key data parameters were extracted and evaluated across studies and treatment types. RESULTS Strong evidence exists for the use probiotic agents to improve symptoms for allergic rhinitis, chronic rhinosinusitis and certain dental conditions. Despite promising results, further investigation is needed to evaluate and optimize probiotic delivery for mitigating otitis media, oropharyngeal inflammation and upper respiratory tract infections. Preclinical studies suggest that probiotics may potentially offer benefit for voice prosthesis maintenance, wound healing and mitigation of oral dysplasia. CONCLUSION Probiotic therapies may offer clinical benefit in a variety of contexts within the field of otolaryngology, especially for short-term relief of certain inflammatory conditions of the oral cavity, auditory and nasal cavities. Further investigation is warranted for evaluation of long-term outcomes and pathogenic deterrence.
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Affiliation(s)
- Alexandra T Bourdillon
- Division of Otolaryngology, Department of Surgery, Yale University School of Medicine, New Haven, CT, United States of America.
| | - Heather A Edwards
- Department of Otolaryngology, Boston University School of Medicine, Boston, MA, United States of America.
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Zommiti M, Feuilloley MGJ, Connil N. Update of Probiotics in Human World: A Nonstop Source of Benefactions till the End of Time. Microorganisms 2020; 8:E1907. [PMID: 33266303 PMCID: PMC7760123 DOI: 10.3390/microorganisms8121907] [Citation(s) in RCA: 97] [Impact Index Per Article: 19.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/18/2020] [Revised: 11/23/2020] [Accepted: 11/23/2020] [Indexed: 02/06/2023] Open
Abstract
Lactic acid bacteria (LAB) are known for their biotechnological potential. Moreover, LAB are distinguished by amazing criteria: Adjusting the intestinal environment, inhibiting pathogenic microbes in the gastrointestinal tract, ability to reduce pathogen adhesion activity, improving the balance of the microbiota inside the intestine, capabilities of regulating intestinal mucosal immunity, and maintaining intestinal barrier function. The escalating number of research and studies about beneficial microorganisms and their impact on promoting health has attracted a big interest in the last decades. Since antiquity, various based fermented products of different kinds have been utilized as potential probiotic products. Nevertheless, the current upsurge in consumers' interest in bioalternatives has opened new horizons for the probiotic field in terms of research and development. The present review aims at shedding light on the world of probiotics, a continuous story of astonishing success in various fields, in particular, the biomedical sector and pharmaceutical industry, as well as to display the importance of probiotics and their therapeutic potential in purpose to compete for sturdy pathogens and to struggle against diseases and acute infections. Shadows and future trends of probiotics use are also discussed.
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Affiliation(s)
- Mohamed Zommiti
- Unité de Protéomique Fonctionnelle et Potentiel Nutraceutique de la Biodiversité de Tunisie, Institut Supérieur des Sciences Biologiques Appliquées de Tunis, Université Tunis El-Manar, Tunis 1006, Tunisia
| | - Marc G. J. Feuilloley
- Laboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Université de Rouen Normandie, Normandie Université, F-27000 Evreux, France; (M.G.J.F.); (N.C.)
| | - Nathalie Connil
- Laboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Université de Rouen Normandie, Normandie Université, F-27000 Evreux, France; (M.G.J.F.); (N.C.)
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Zhao W, Liu Y, Kwok LY, Cai T, Zhang W. The immune regulatory role of Lactobacillus acidophilus: An updated meta-analysis of randomized controlled trials. FOOD BIOSCI 2020. [DOI: 10.1016/j.fbio.2020.100656] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/30/2023]
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Sadeghi-Shabestari M, Jabbari Moghaddam Y, Rezapoor H, Sohrabpour M. Effect of Probiotics on Allergic Rhinitis: A Randomized, Controlled, Clinical Trial. Galen Med J 2020; 9:e1918. [PMID: 34466612 PMCID: PMC8343930 DOI: 10.31661/gmj.v9i0.1918] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/28/2020] [Revised: 06/13/2020] [Accepted: 06/13/2020] [Indexed: 12/02/2022] Open
Abstract
Background: Allergic rhinitis (AR) is one of the most common diseases in the world and affects about 10-50% of the general population. Probiotics are live microorganisms that help the normal state of the intestine, and if prescribed correctly, they can stimulate the mucosal immune system to prevent inflammatory symptoms of allergy and atopy. The present study aims to investigate the role of probiotics in the treatment of AR when added to standard therapy as adjuvant agents. Materials and Methods: In this clinical trial study, 28 patients older than 15 years with AR randomly divided into probiotics and control groups. The probiotics group received standard therapy for AR accompanied by probiotic capsules every 12 hours for eight weeks, whereas the control group received standard therapy for AR with placebo capsules as the same protocol. Data were analyzed using SPSS Version 23 (IBM Corporation, Armonk, NY, USA) and, the P-value less than 0.05 was considered statistically significant. Results: In the probiotics group, 14.3% of patients had sneezing at the baseline, which significantly decreased to 4.6% (P<0.01). Also, the necessity for nasal and oral corticosteroids after treatment with probiotics in the probiotics group was less than the control group (P<0.01). Although cough, nasal discharge, conchae hypertrophy, and night sleep disorders reduced after treatment with probiotics, this reduction was not statistically significant between the two groups. Conclusion: Based on the results of this clinical trial, the use of probiotics had no significant effect on the outcome of patients with AR.
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Affiliation(s)
- Mahnaz Sadeghi-Shabestari
- Immunology Research Center of Tabriz, TB and lung Research Center of Tabriz, Tabriz University of Medical Sciences, Tabriz, Iran
| | - Yalda Jabbari Moghaddam
- ENT Department, Tabriz University of Medical Sciences, Tabriz, Iran
- Correspondence to: Associated Professor of Otolaryngology of Tabriz University of Medical Sciences, Iran Telephone Number: +984133352076 Email Address:
| | - Hasan Rezapoor
- ENT Department, Tabriz University of Medical Sciences, Tabriz, Iran
| | - Mojataba Sohrabpour
- Noncommunicable Diseases Research Center, Fasa University of Medical Sciences, Fasa, Iran
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19
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Kang MG, Han SW, Kang HR, Hong SJ, Kim DH, Choi JH. Probiotic NVP-1703 Alleviates Allergic Rhinitis by Inducing IL-10 Expression: A Four-week Clinical Trial. Nutrients 2020; 12:nu12051427. [PMID: 32429063 PMCID: PMC7284371 DOI: 10.3390/nu12051427] [Citation(s) in RCA: 21] [Impact Index Per Article: 4.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/27/2020] [Revised: 05/11/2020] [Accepted: 05/12/2020] [Indexed: 12/18/2022] Open
Abstract
Although several recent studies reported that probiotics might be beneficial for allergic rhinitis (AR), the effect of probiotics on AR is not consistent and have not been reproduced between studies. We aimed to determine the efficacy and safety of probiotic NVP-1703, a mixture of Bifidobacterium longum and Lactobacillus plantarum, in subjects with perennial AR. Adult subjects with perennial AR received either NVP-1703 (n = 47) or placebo (n = 48) for four weeks. Total nasal symptom scores (TNSS), rhinitis control assessment test (RCAT), blood eosinophil count, allergen-specific IgE, and immunological parameters in serum and urine were compared at baseline and after four weeks. TNSS changes from baseline at weeks 1, 3, and 4 were significant between the NVP-1703 and placebo groups (p = 0.033, 0.031, and 0.029, respectively). RCAT score showed significant differences between the NVP-1703 and placebo groups (p = 0.049) at week 4. Dermatophagoides farinae-specific IgE levels and serum IL-10 levels were significantly different between the NVP-1703 and placebo groups (p = 0.033 and p = 0.047, respectively). IL-10/IL-4 and IL-10/IL-13 ratios were different between the NVP-1703 and placebo groups at week 4 (p = 0.046 and 0.018, respectively). NVP-1703 treatment reduced urinary prostaglandin F2α and leukotriene E4 levels (p > 0.05). Therefore, NVP-1703 can be treatment option for perennial AR.
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Affiliation(s)
- Min-Gyu Kang
- Department of Allergy and Clinical Immunology, Chungbuk National University Hospital, Cheongju 28644, Korea;
- Department of Internal Medicine, Chungbuk National University College of Medicine, Cheongju 28644, Korea
| | - Seung-Won Han
- PB Business Department, Navipharm Inc., Suwon 16209, Korea;
| | - Hye-Ryun Kang
- Department of Internal Medicine, Division of Allergy and Clinical Immunology, Seoul National University Hospital, Seoul 03080, Korea;
| | - Seok-Jin Hong
- Department of Otorhinolaryngology—Head and Neck Surgery, Hallym University Dongtan Sacred Heart Hospital, Hwaseong 18450, Korea;
- Allergy and Clinical Immunology Research Center, Hallym University College of Medicine, Chuncheon 24252, Korea
| | - Dong-Hyun Kim
- Neurobiota Research Center, College of Pharmacy, Kyung Hee University, Seoul 02453, Korea;
| | - Jeong-Hee Choi
- Allergy and Clinical Immunology Research Center, Hallym University College of Medicine, Chuncheon 24252, Korea
- Department of Pulmonology and Allergy, Hallym University Dongtan Sacred Heart Hospital, Hwaseong 18450, Korea
- Correspondence: ; Tel.: +82-31-8086-2928; Fax: +82-31-8086-2482
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Feleszko W, Rossi GA, Krenke R, Canonica GW, Van Gerven L, Kalyuzhin O. Immunoactive preparations and regulatory responses in the respiratory tract: potential for clinical application in chronic inflammatory airway diseases. Expert Rev Respir Med 2020; 14:603-619. [PMID: 32250709 DOI: 10.1080/17476348.2020.1744436] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/24/2022]
Abstract
Introduction: The prevalence of chronic inflammatory airway diseases is rising. Their treatment with corticosteroids increases infection risk, while overuse of antimicrobial agents may increase morbidity and antimicrobial resistance. Nonspecific immunomodulatory compounds alter immune responses to both infectious and atopic challenges. These compounds may offer an alternative approach for symptom reduction and prophylaxis against both infections and exacerbations in chronic inflammatory airway disease.Areas covered: We assessed the available data on the efficacy of nonspecific immunomodulators including bacterial lysates, synthetic compounds, and vaccines in chronic rhinosinusitis (CRS); allergic and non-allergic rhinitis; chronic obstructive pulmonary disease (COPD), and asthma. A search of PubMed was carried out using the 'Clinical Trials' filter for each condition and immunomodulatory product detailed below, where available, data from meta-analyses were reported.Expert opinion: Pre-clinical data has revealed a coherent mechanistic path of action for oral immunomodulators on the respiratory immune system, principally via the gut-lung immune axis. In patients with asthma, allergic rhinitis, CRS, and COPD immunomodulatory therapy reduces symptoms, exacerbations, hospitalizations, and drug consumption. However, data are heterogeneous, and study quality remains limited. A lack of high-quality recent trials remains the major unmet research need in the field.
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Affiliation(s)
- Wojciech Feleszko
- Department of Pediatric Respiratory Diseases and Allergy, The Medical University of Warsaw, Warsaw, Poland
| | - Giovanni A Rossi
- Chief Emeritus, Pediatric Pulmonology and Allergy Units, Cystic Fibrosis Regional Centre, IRCCS G. Gaslini, Genoa, Italy
| | - Rafal Krenke
- Department of Internal Medicine, Pulmonary Diseases & Allergy, Medical University of Warsaw, Warsaw, Poland
| | - G Walter Canonica
- Personalized Medicine Asthma & Allergy, Clinic-Humanitas University & Research Hospital, Milan, Italy
| | - Laura Van Gerven
- Department of Otorhinolaryngology, Head and Neck Surgery, University Hospitals Leuven, Leuven, Belgium
| | - Oleg Kalyuzhin
- Professor of Department of Clinical Immunology and Allergy, I.M. Sechenov First Moscow State Medical University of the Ministry of Health of the Russian Federation (Sechenov University), Moscow, Russia
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Oral and nasal probiotic administration for the prevention and alleviation of allergic diseases, asthma and chronic obstructive pulmonary disease. Nutr Res Rev 2020; 34:1-16. [PMID: 32281536 DOI: 10.1017/s0954422420000116] [Citation(s) in RCA: 28] [Impact Index Per Article: 5.6] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/17/2022]
Abstract
Interaction between a healthy microbiome and the immune system leads to body homeostasis, as dysbiosis in microbiome content and loss of diversity may result in disease development. Due to the ability of probiotics to help and modify microbiome constitution, probiotics are now widely used for the prevention and treatment of different gastrointestinal, inflammatory, and, more recently, respiratory diseases. In this regard, chronic respiratory diseases including chronic obstructive pulmonary disease (COPD), asthma and allergic rhinitis are among the most common and complicated respiratory diseases with no specific treatment until now. Accordingly, many studies have evaluated the therapeutic efficacy of probiotic administration (mostly via the oral route and much lesser nasal route) on chronic respiratory diseases. We tried to summarise and evaluate these studies to give a perspective of probiotic therapy via both the oral and nasal routes for respiratory infections (in general) and chronic respiratory diseases (specifically). We finally concluded that probiotics might be useful for allergic diseases. For asthmatic patients, probiotics can modulate serum cytokines and IgE and decrease eosinophilia, but with no significant reduction in clinical symptoms. For COPD, only limited studies were found with uncertain clinical efficacy. For intranasal administration, although some studies propose more efficiency than the oral route, more clinical evaluations are warranted.
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Sestito S, D'Auria E, Baldassarre ME, Salvatore S, Tallarico V, Stefanelli E, Tarsitano F, Concolino D, Pensabene L. The Role of Prebiotics and Probiotics in Prevention of Allergic Diseases in Infants. Front Pediatr 2020; 8:583946. [PMID: 33415087 PMCID: PMC7783417 DOI: 10.3389/fped.2020.583946] [Citation(s) in RCA: 46] [Impact Index Per Article: 9.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/16/2020] [Accepted: 11/23/2020] [Indexed: 12/15/2022] Open
Abstract
Allergic diseases have been linked to genetic and/or environmental factors, such as antibiotic use, westernized high fat and low fiber diet, which lead to early intestinal dysbiosis, and account for the rise in allergy prevalence, especially in western countries. Allergic diseases have shown reduced microbial diversity, including fewer lactobacilli and bifidobacteria, within the neonatal microbiota, before the onset of atopic diseases. Raised interest in microbiota manipulating strategies to restore the microbial balance for atopic disease prevention, through prebiotics, probiotics, or synbiotics supplementation, has been reported. We reviewed and discussed the role of prebiotics and/or probiotics supplementation for allergy prevention in infants. We searched PubMed and the Cochrane Database using keywords relating to "allergy" OR "allergic disorders," "prevention" AND "prebiotics" OR "probiotics" OR "synbiotics." We limited our evaluation to papers of English language including children aged 0-2 years old. Different products or strains used, different period of intervention, duration of supplementation, has hampered the draw of definitive conclusions on the clinical impact of probiotics and/or prebiotics for prevention of allergic diseases in infants, except for atopic dermatitis in infants at high-risk. This preventive effect on eczema in high-risk infants is supported by clear evidence for probiotics but only moderate evidence for prebiotic supplementation. However, the optimal prebiotic or strain of probiotic, dose, duration, and timing of intervention remains uncertain. Particularly, a combined pre- and post-natal intervention appeared of stronger benefit, although the definition of the optimal intervention starting time during gestation, the timing, and duration in the post-natal period, as well as the best target population, are still an unmet need.
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Affiliation(s)
- Simona Sestito
- Pediatric Unit, Department of Medical and Surgical Sciences, University "Magna Graecia" of Catanzaro, Catanzaro, Italy
| | - Enza D'Auria
- Department of Pediatrics, Vittore Buzzi Children's Hospital-University of Milan, Milan, Italy
| | - Maria Elisabetta Baldassarre
- Neonatology and Neonatal Intensive Care Unit, Department of Biomedical Science and Human Oncology, "Aldo Moro" University of Bari, Bari, Italy
| | - Silvia Salvatore
- Department of Pediatrics, Ospedale "F. Del Ponte", University of Insubria, Varese, Italy
| | - Valeria Tallarico
- Pediatric Unit, Department of Medical and Surgical Sciences, University "Magna Graecia" of Catanzaro, Catanzaro, Italy
| | - Ettore Stefanelli
- Pediatric Unit, Department of Medical and Surgical Sciences, University "Magna Graecia" of Catanzaro, Catanzaro, Italy
| | - Flora Tarsitano
- Pediatric Unit, Department of Medical and Surgical Sciences, University "Magna Graecia" of Catanzaro, Catanzaro, Italy
| | - Daniela Concolino
- Pediatric Unit, Department of Medical and Surgical Sciences, University "Magna Graecia" of Catanzaro, Catanzaro, Italy.,Department of Health Sciences, School of Medicine and Surgery, University Magna Graecia of Catanzaro, Catanzaro, Italy
| | - Licia Pensabene
- Pediatric Unit, Department of Medical and Surgical Sciences, University "Magna Graecia" of Catanzaro, Catanzaro, Italy
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Schaefer M, Enck P. Effects of a probiotic treatment ( Enterococcus faecalis) and open-label placebo on symptoms of allergic rhinitis: study protocol for a randomised controlled trial. BMJ Open 2019; 9:e031339. [PMID: 31662387 PMCID: PMC6830672 DOI: 10.1136/bmjopen-2019-031339] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/29/2019] [Revised: 09/03/2019] [Accepted: 09/18/2019] [Indexed: 12/13/2022] Open
Abstract
INTRODUCTION Several studies suggest that gut microbiota may play an important role in allergic diseases. The present trial aims to examine effects of the probiotic Enterococcus faecalis on symptoms of allergic rhinitis in patients. Effects of this probiotic on the immune system have been reported by several studies, but the majority of the previous trials were animal studies. In addition, it is well known that symptoms in allergic rhinitis are prone to exhibit high placebo responses. Moreover, recent studies report that even placebos without deception (open-label placebos) are highly effective in reducing symptoms of allergic rhinitis. Our study design combines both new approaches to assess effects on allergic symptoms in patients. The objective of this study is to compare the effects of a probiotic treatment (E. faecalis) with effects seen by open-label placebo, concealed placebo treatment and no treatment control. METHODS AND ANALYSIS A total of 120 patients with allergic rhinitis will be randomly assigned to one of four different groups: a double-blind probiotic/placebo group (groups 1 and 2), an open-label placebo group (group 3) and a no-treatment group (group 4) to control for spontaneous variation of symptoms. The primary outcome is the evaluation of allergic symptoms using the Combined Symptoms Medication Score. Furthermore, health-related quality of life is examined (Rhinitis Quality of Life Questionnaire). Secondary outcomes include a visual analogue scale on allergic burden and a second quality of life questionnaire. This report describes the study design of the randomised controlled trial. ETHICS AND DISSEMINATION The study design was approved by the ethical committee of the UKT Department of Psychosomatic Medicine and Psychotherapy, Tübingen, Germany. The trial is registered at the German Clinical Trials Register (www.drks.de, DRKS00015804). The trial results will be published in peer-reviewed journals and at conferences. TRIAL REGISTRATION NUMBER German Clinical Trials Register (www.drks.de, DRKS00015804); Pre-results.
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Affiliation(s)
- Michael Schaefer
- Department Naturwissenschaften, Medical School Berlin, Berlin, Germany
| | - Paul Enck
- Department of Internal Medicine VI: Psychosomatic Medicine and Psychotherapy, University of Tubingen, Tübingen, Germany
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Martens K, Pugin B, De Boeck I, Spacova I, Steelant B, Seys SF, Lebeer S, Hellings PW. Probiotics for the airways: Potential to improve epithelial and immune homeostasis. Allergy 2018; 73:1954-1963. [PMID: 29869783 DOI: 10.1111/all.13495] [Citation(s) in RCA: 53] [Impact Index Per Article: 7.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 05/29/2018] [Indexed: 12/30/2022]
Abstract
Probiotics are live microorganisms that, when administered in adequate amounts, confer health benefit on the host. The therapeutic effects of probiotics have been mostly studied in the gastrointestinal tract, but recent evidence points toward the potential of these bacteria to prevent and/or treat chronic airway diseases. In this review, possible mechanisms of action of probiotics in the airways are described, with a particular focus on their capacity to modulate the epithelial barrier function and their mode of interaction with the immune system. Indeed, probiotic bacteria, mostly lactobacilli, can promote the expression and regulation of tight junctions and adherence junctions, resulting in the restoration of a defective epithelial barrier. These bacteria interact with the epithelial barrier and immune cells through pattern recognition receptors, such as Toll-like receptors, which upon activation can stimulate or suppress various immune responses. Finally, the clinical potential of probiotics to treat inflammatory diseases of the upper and lower respiratory tract, and the difference between their mode of application (eg, oral or nasal) are discussed here.
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Affiliation(s)
- K. Martens
- Clinical Immunology Department of Microbiology and Immunology KU Leuven Leuven Belgium
| | - B. Pugin
- Clinical Immunology Department of Microbiology and Immunology KU Leuven Leuven Belgium
| | - I. De Boeck
- Department of Bioscience Engineering University of Antwerp Antwerp Belgium
| | - I. Spacova
- Department of Bioscience Engineering University of Antwerp Antwerp Belgium
| | - B. Steelant
- Clinical Immunology Department of Microbiology and Immunology KU Leuven Leuven Belgium
| | - S. F. Seys
- Clinical Immunology Department of Microbiology and Immunology KU Leuven Leuven Belgium
| | - S. Lebeer
- Department of Bioscience Engineering University of Antwerp Antwerp Belgium
| | - P. W. Hellings
- Clinical Immunology Department of Microbiology and Immunology KU Leuven Leuven Belgium
- Clinical Division of Otorhinolaryngology, Head and Neck Surgery University Hospitals Leuven Leuven Belgium
- Department of Otorhinolaryngology University Hospitals Ghent Ghent Belgium
- Department of Otorhinolaryngology Academic Medical Center University of Amsterdam Amsterdam the Netherlands
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Material distributions and functional structures in probiotic microcapsules. Eur J Pharm Sci 2018; 122:1-8. [DOI: 10.1016/j.ejps.2018.06.013] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/24/2018] [Revised: 05/23/2018] [Accepted: 06/13/2018] [Indexed: 11/23/2022]
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Lin J, Zhang Y, He C, Dai J. Probiotics supplementation in children with asthma: A systematic review and meta-analysis. J Paediatr Child Health 2018; 54:953-961. [PMID: 30051941 DOI: 10.1111/jpc.14126] [Citation(s) in RCA: 32] [Impact Index Per Article: 4.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/20/2018] [Revised: 05/15/2018] [Accepted: 06/07/2018] [Indexed: 12/15/2022]
Abstract
AIM To systematically review the effects of probiotics supplementation in children with asthma. METHODS An electronic search was conducted on PubMed, Embase, Cochrane Central Register of Controlled Trials, China National Knowledge Infrastructure Database, CQ VIP Database and Wanfang Data until November 2017. The reference lists of included studies and pertinent reviews were checked for supplementing our search. Randomised control trials that compared probiotics versus placebo were included. RESULTS Eleven studies with a total of 910 children met eligibility criteria. The pooled data revealed that the proportion of children with fewer episodes of asthma was significantly higher in the probiotics group than in the control group (risk ratio 1.3, 95% confidence interval (CI) 1.06-1.59); the reduction of IL-4 (mean differences -2.34, 95% CI -3.38, -1.29) and the increasing of interferon-γ (mean differences 2.5, 95% CI 1.23-3.76) was also significant after the treatment of probiotics. Nevertheless, no statistical significance was observed in childhood asthma control test, asthmatic symptom in the day and night, the number of symptom-free days, forced expiratory volume in the first second predicted and peak expiratory flow. CONCLUSIONS This systematic review does not confirm or rule out the beneficial effects of probiotics supplementation in children with asthma. More well-designed randomised control trials with larger sample sizes need to be conducted to evaluate the effects of probiotics in children with asthma in the future.
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Affiliation(s)
- Jilei Lin
- Respiratory Department, Children's Hospital, Chongqing Medical University, Chongqing, China.,Ministry of Education Key Laboratory of Child Development and Disorders, Children's Hospital, Chongqing Medical University, Chongqing, China
| | - Yin Zhang
- Respiratory Department, Children's Hospital, Chongqing Medical University, Chongqing, China
| | - Chunyan He
- Respiratory Department, Children's Hospital, Chongqing Medical University, Chongqing, China.,Ministry of Education Key Laboratory of Child Development and Disorders, Children's Hospital, Chongqing Medical University, Chongqing, China
| | - Jihong Dai
- Respiratory Department, Children's Hospital, Chongqing Medical University, Chongqing, China.,Ministry of Education Key Laboratory of Child Development and Disorders, Children's Hospital, Chongqing Medical University, Chongqing, China
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Lee SY, Lee E, Park YM, Hong SJ. Microbiome in the Gut-Skin Axis in Atopic Dermatitis. ALLERGY, ASTHMA & IMMUNOLOGY RESEARCH 2018; 10:354-362. [PMID: 29949831 PMCID: PMC6021588 DOI: 10.4168/aair.2018.10.4.354] [Citation(s) in RCA: 180] [Impact Index Per Article: 25.7] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 11/15/2017] [Revised: 12/16/2017] [Accepted: 12/29/2017] [Indexed: 01/01/2023]
Abstract
The microbiome is vital for immune system development and homeostasis. Changes in microbial composition and function, termed dysbiosis, in the skin and the gut have recently been linked to alterations in immune responses and to the development of skin diseases, such as atopic dermatitis (AD). In this review, we summarize the recent findings on the gut and skin microbiome, highlighting the roles of major commensals in modulating skin and systemic immunity in AD. Although our understanding of the gut-skin axis is only beginning, emerging evidence indicates that the gut and skin microbiome could be manipulated to treat AD.
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Affiliation(s)
- So Yeon Lee
- Department of Pediatrics, Childhood Asthma Atopy Center, Environmental Health Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Eun Lee
- Department of Pediatrics, Chonnam National University Hospital, Chonnam National University Medical School, Gwangju, Korea
| | - Yoon Mee Park
- Asan Institute for Life Science, University of Ulsan College of Medicine, Seoul, Korea
| | - Soo Jong Hong
- Department of Pediatrics, Childhood Asthma Atopy Center, Environmental Health Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea.
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Rondanelli M, Faliva MA, Perna S, Giacosa A, Peroni G, Castellazzi AM. Using probiotics in clinical practice: Where are we now? A review of existing meta-analyses. Gut Microbes 2017; 8. [PMID: 28640662 PMCID: PMC5730384 DOI: 10.1080/19490976.2017.1345414] [Citation(s) in RCA: 100] [Impact Index Per Article: 12.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/08/2023] Open
Abstract
The scientific literature has demonstrated that probiotics have a broad spectrum of activity, although often the results are contradictory. This study provides a critical overview of the current meta-analyses that have evaluated the efficacy of probiotics in physiologic and pathological conditions, such as metabolic disease, antibiotic-associated and Clostridium difficile-associated diarrhea, IBS, constipation, IBD, chemotherapy-associated diarrhea, respiratory tract infection, ventilator-associated pneumonia, NAFLD, liver encephalopathy, periodontitis, depression, vaginosis, urinary tract infections, pancreatitis, incidence of ventilator-associated pneumonia, hospital infection and stay in ICU, mortality of post-trauma patients, necrotising enterocolitis in premature infants. Only for antibiotic- and Clostridium difficile-associated diarrhea, and respiratory tract infections the effects of probiotics are considered "evidence-based." Concerning other fields, meta-analyses lacks to define type and biologic effect of probiotic strains, as well as the outcome in a disease state. Therefore, the results presented should be a stimulus for further studies which will provide clinical recommendations.
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Affiliation(s)
- Mariangela Rondanelli
- Department of Applied Health Sciences, Azienda di Servizi alla Persona (ASP) di Pavia, University of Pavia, Pavia, Italy
| | - Milena Anna Faliva
- Department of Applied Health Sciences, Azienda di Servizi alla Persona (ASP) di Pavia, University of Pavia, Pavia, Italy
| | - Simone Perna
- Department of Applied Health Sciences, Azienda di Servizi alla Persona (ASP) di Pavia, University of Pavia, Pavia, Italy,CONTACT Simone Perna, , Department of Public Health, Experimental and Forensic Medicine, School of Medicine, University of Pavia, Endocrinology and Nutrition Unit, Azienda di Servizi alla Persona di Pavia, Pavia, Italy
| | - Attilio Giacosa
- Department of Gastroenterology, Policlinico di Monza, Monza, Italy and Centro Diagnostico Italiano, Milan, Italy
| | - Gabriella Peroni
- Department of Applied Health Sciences, Azienda di Servizi alla Persona (ASP) di Pavia, University of Pavia, Pavia, Italy
| | - Anna Maria Castellazzi
- Castellazzi Department of Clinical Surgical Diagnostic and Pediatric Sciences, University of Pavia, Pavia, Italy
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Güvenç IA, Muluk NB, Mutlu FŞ, Eşki E, Altıntoprak N, Oktemer T, Cingi C. Do probiotics have a role in the treatment of allergic rhinitis? A comprehensive systematic review and meta-analysis. Am J Rhinol Allergy 2016; 30:157-175. [PMID: 27442711 DOI: 10.2500/ajra.2016.30.4354] [Citation(s) in RCA: 53] [Impact Index Per Article: 5.9] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/04/2023]
Abstract
OBJECTIVE To investigate clinical evidence for the efficacy of probiotics in the treatment of allergic rhinitis (AR). METHODS A systematic search was conducted to review the results of all randomized, double-blind, placebo-controlled trials by following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Statement. Primary outcome measurements were total nasal and ocular symptom scores (SS) and quality of life (QoL) questionnaires. Secondary outcome measurements were individual nasal SS and immunologic parameters. RESULTS Twenty-two randomized, double-blind, placebo-controlled studies were included. Seventeen trials showed significant benefit of probiotics clinically, whereas eight trials showed significant improvement in immunologic parameters compared with placebo. All five studies with Lactobacillus paracasei (LP) strains demonstrated clinically significant improvements compared with placebo. Probiotics showed significant reduction in nasal and ocular SS (standardized mean difference [SMD], -1.23, p < 0.001; and SMD, -1.84, p < 0.001; respectively), total, nasal, and ocular QoL scores compared with placebo (SMD, -1.84, p < 0.001; SMD, -2.30, p = 0.006; and SMD, -3.11, p = 0.005; respectively). Although heterogeneity was high, in subgroup analysis, SMD for total nasal and ocular symptoms with patients with seasonal AR and for nasal QoL scores for studies with LP-33 strain were significant and homogenous. Scores of nasal blockage, rhinorrhea, and nasal itching were significantly lower in the probiotic group compared with placebo. The meta-analysis studies SS the Japanese guidelines revealed a significant, homogenous SMD score of -0.34 for individual nasal SS, above the minimal important clinical difference value of 0.3. The T-helper 1 to T-helper 2 ratio was significantly lower in the probiotic group compared with placebo (SMD, -0.78; p = 0.045). CONCLUSION Despite high variability among the studies, synthesis of available data provided significant evidence of beneficial clinical and immunologic effects of probiotics in the treatment of AR, especially with seasonal AR and LP-33 strains. With the rising pool of studies, the most promising strains in specific allergies can be revealed and adjuvant therapy with probiotics can be recommended for the treatment of AR.
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Affiliation(s)
- Işıl Adadan Güvenç
- Department of Otorhinolaryngology, Çigli Regional Education Hospital, İzmir, Turkey
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Turner JH, Adams AS, Zajac A. Probiotics in prevention and treatment of allergic rhinitis. Am J Rhinol Allergy 2016; 29:e224. [PMID: 26637575 DOI: 10.2500/ajra.2015.29.4257] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [MESH Headings] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022]
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Abstract
The gastrointestinal (GI) tract microbiota is required for optimal digestion of foods, for the development of resistance against pathogens (termed colonization resistance), for the development of mucosa-associated lymphoid tissue, and for local as well as systemic immune homeostasis. Certain constituents of the GI tract microbiota are widely recognized as critical regulators and modulators of their host's immune response. These include bacterial members of the microbiota as well as parasitic nematodes. Immune regulation by immunomodulatory members of the GI microbiota primarily serves to subvert host antimicrobial immune defenses and promote persistent colonization, but as a side effect may prevent or suppress immunological disorders resulting from inappropriate responses to harmless antigens, such as allergy, colitis or autoimmunity. Many of the best understood GI-resident immunomodulatory species have co-evolved with their mammalian hosts for tens of thousands of years and masterfully manipulate host immune responses. In this review, we discuss the epidemiological evidence for the role of the GI tract microbiota as a whole, and of specific members, in protection against allergic and other immunological disorders. We then focus on the mechanistic basis of microbial immunomodulation, which is presented using several well-understood paradigmatic examples, that is, helminths, Helicobacter pylori, Bifidobacteria and Lactobacilli. In a final chapter, we highlight past and ongoing attempts at harnessing the immunomodulatory properties of GI microbiota species and their secreted products for intervention studies and describe the promises and limitations of these experimental approaches. The effects of pro- and prebiotics, bacterial lysates, as well as of fecal microbiota transplantation are presented and compared.
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Affiliation(s)
- Andreas Kyburz
- Institute of Molecular Cancer Research, University of Zurich, Winterthurerstr, Zurich, Switzerland
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Turner J. Advancing the understanding of complex rhinologic problems. Am J Rhinol Allergy 2015; 29:233-4. [PMID: 26163242 DOI: 10.2500/ajra.2015.29.4226] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/20/2022]
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