The Impact of Synbiotics on the Bacterial Flora During the Course of Chronic Sinusitis
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Population
- Diagnosis of CRS according to EPOS 2020 guidelines
- Qualification for endoscopic sinus surgery
- Secondary CRS according to EPOS 2020
- Benign and malignant neoplasms of the sinuses
- Immunosuppressive treatment
- Age under 18 years
- Lack of qualification for general anesthesia
- Mental or physical condition preventing completion of questionnaires
- Pregnancy
- Unilateral lesions
- Infection within 6 weeks prior to surgery
- Antibiotic therapy within 6 weeks prior to surgery
- Surgery performed during the pollen season in patients allergic to pollen or mold spores
2.2. Methodology
- Probiotics: Lactobacillus acidophilus, Lactobacillus casei, Lactobacillus plantarum, Lactobacillus rhamnosus, Lactobacillus delbrueckii subsp. bulgaricus, Bifidobacterium bifidum, Bifidobacterium breve, Bifidobacterium longum, Streptococcus thermophilus
- Prebiotic: Fructooligosaccharides
2.3. Bacteriological Procedures
2.4. Laboratory Procedures
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
CRS | Chronic Rhinosinusitis |
AR | Allergic Rhinitis |
ESS | Endoscopic Sinus Surgery |
EPOS 2020 | European Position Paper on Rhinosinusitis and Nasal Polyps 2020 |
MRSA | Methicillin-Resistant Staphylococcus aureus |
MSSA | Methicillin-Sensitive Staphylococcus aureus |
NSAID | Non-Steroidal Anti-Inflammatory Drug |
CRSwNP | Chronic Rhinosinusitis with Nasal Polyps |
CRSsNP | Chronic Rhinosinusitis without Nasal Polyps |
VAS | Visual Analog Scale |
SNOT-22 | Sino-Nasal Outcome Test-22 |
References
- Sedaghat, A.R.; Kuan, E.C.; Scadding, G.K. Epidemiology of Chronic Rhinosinusitis: Prevalence and Risk Factors. J. Allergy Clin. Immunol. Pr. 2022, 10, 1395–1403. [Google Scholar] [CrossRef] [PubMed]
- Rudmik, L. Economics of Chronic Rhinosinusitis. Curr. Allergy Asthma. Rep. 2017, 17, 20. [Google Scholar] [CrossRef] [PubMed]
- Kato, Y.; Matsumura, Y. Role of Microbiota in Atopic Dermatitis and Bronchial Asthma—Triangular Cross-Talk among Skin, Airway and Gut. Arch. Clin. Biomed. Res. 2020, 4, 169–183. [Google Scholar] [CrossRef]
- Paramasivan, S.; Bassiouni, A.; Shiffer, A.; Dillon, M.R.; Cope, E.K.; Cooksley, C.; Ramezanpour, M.; Moraitis, S.; Ali, M.J.; Bleier, B.; et al. The international sinonasal microbiome study: A multicentre, multinational characterization of sinonasal bacterial ecology. Allergy 2020, 75, 2037–2049. [Google Scholar] [CrossRef] [PubMed]
- Bomar, L.; Brugger, S.D.; Yost, B.H.; Davies, S.S.; Lemon, K.P. Corynebacterium accolens Releases Antipneumococcal Free Fatty Acids from Human Nostril and Skin Surface Triacylglycerols. mBio 2016, 7, e01725-15. [Google Scholar] [CrossRef] [PubMed]
- Alagiakrishnan, K.; Morgadinho, J.; Halverson, T. Approach to the diagnosis and management of dysbiosis. Front. Nutr. 2024, 11, 1330903. [Google Scholar] [CrossRef] [PubMed]
- Lim, S.J.; Jithpratuck, W.; Wasylik, K.; Sriaroon, P.; Dishaw, L.J. Associations of Microbial Diversity with Age and Other Clinical Variables among Pediatric Chronic Rhinosinusitis (CRS) Patients. Microorganisms 2023, 11, 422. [Google Scholar] [CrossRef] [PubMed]
- Koeller, K.; Herlemann, D.P.R.; Schuldt, T.; Ovari, A.; Guder, E.; Podbielski, A.; Kreikemeyer, B.; Olzowy, B. Microbiome and Culture Based Analysis of Chronic Rhinosinusitis Compared to Healthy Sinus Mucosa. Front. Microbiol. 2018, 9, 643. [Google Scholar] [CrossRef] [PubMed]
- Dimitri-Pinheiro, S.; Soares, R.; Barata, P. The Microbiome of the Nose-Friend or Foe? Allergy Rhinol. 2020, 11, 2152656720911605. [Google Scholar] [CrossRef] [PubMed]
- Lal, D.; Keim, P.; Delisle, J.; Barker, B.; Rank, M.A.; Chia, N.; Schupp, J.M.; Gillece, J.D.; Cope, E.K. Mapping and comparing bacterial microbiota in the sinonasal cavity of healthy, allergic rhinitis, and chronic rhinosinusitis subjects. Int. Forum. Allergy Rhinol. 2017, 7, 561–569. [Google Scholar] [CrossRef] [PubMed]
- Baud, D.; Dimopoulou Agri, V.; Gibson, G.R.; Reid, G.; Giannoni, E. Using Probiotics to Flatten the Curve of Coronavirus Disease COVID-2019 Pandemic. Front. Public Health 2020, 8, 186. [Google Scholar] [CrossRef] [PubMed]
- Harata, G.; He, F.; Hiruta, N.; Kawase, M.; Kubota, A.; Hiramatsu, M.; Yausi, H. Intranasal administration of Lactobacillus rhamnosus GG protects mice from H1N1 influenza virus infection by regulating respiratory immune responses. Lett. Appl. Microbiol. 2010, 50, 597–602. [Google Scholar] [CrossRef] [PubMed]
- Standyło, A.; Obuchowska, A.; Horaczyńska-Wojtaś, A.; Mielnik-Niedzielska, G. Effects of Probiotic Supplementation during Chronic Rhinosinusitis on the Microbiome. J. Clin. Med. 2024, 13, 1726. [Google Scholar] [CrossRef] [PubMed]
- Chen, P.C.; Hsu, H.Y.; Liao, Y.C.; Lee, C.C.; Hsieh, M.H.; Kuo, W.S.; Wu, L.S.; Wang, J.Y. Oral administration of Lactobacillus delbrueckii subsp. lactis LDL557 attenuates airway inflammation and changes the gut microbiota in a Der p-sensitized mouse model of allergic asthma. Asian Pac. J. Allergy Immunol. 2024. [Google Scholar] [CrossRef] [PubMed]
- Sadrifar, S.; Abbasi-Dokht, T.; Forouzandeh, S.; Malek, F.; Yousefi, B.; Salek Farrokhi, A.; Karami, J.; Baharlou, R. Immunomodulatory effects of probiotic supplementation in patients with asthma: A randomized, double-blind, placebo-controlled trial. Allergy Asthma Clin. Immunol. 2023, 19, 1. [Google Scholar] [CrossRef] [PubMed]
- Sadrifar, S.; Abbasi-Dokht, T.; Forouzandeh, S.; Malek, F.; Baharlou, R. The impact of multistrains of probiotics on Th17-related cytokines in patients with asthma: A randomized, double-blind, placebo-controlled trial. J. Asthma 2023, 60, 1306–1315. [Google Scholar] [CrossRef] [PubMed]
- Abbasi-Dokht, T.; Sadrifar, S.; Forouzandeh, S.; Malek, F.; Hemmati, M.; Kokhaei, P.; Salek Farrokhi, A.; Baharlou, R. Multistrain Probiotics Supplement Alleviates Asthma Symptoms via Increasing Treg Cells Population: A Randomized, Double-Blind, Placebo-Controlled Trial. Int. Arch. Allergy Immunol. 2023, 184, 291–301. [Google Scholar] [CrossRef] [PubMed]
- Moermans, C.; Graff, S.; Medard, L.; Schleich, F.; Paulus, V.; Guissard, F.; Henket, M.; Louis, R. Effects of probiotics in uncontrolled asthma. ERJ Open Res. 2022, 8 (Suppl. S8), 169. [Google Scholar]
- Wahyu, F.; Gayatri, A. Probiotic as supplementary therapy for chronic rhinosinusitis. Int. J. Sci. Res. Updates 2022, 4, 103–107. [Google Scholar] [CrossRef]
- Fong, P.; Lim, K.; Gnanam, A.; Charn, T. Role of probiotics in chronic rhinosinusitis: A systematic review of randomised, controlled trials. J. Laryngol. Otol. 2023, 137, 1300–1311. [Google Scholar] [CrossRef] [PubMed]
- Liu, P.; Hu, T.; Kang, C.; Liu, J.; Zhang, J.; Ran, H.; Zeng, X.; Qiu, S. Research Advances in the Treatment of Allergic Rhinitis by Probiotics. J. Asthma Allergy 2022, 15, 1413–1428. [Google Scholar] [CrossRef] [PubMed]
- Fokkens, W.J.; Lund, V.J.; Hopkins, C.; Hellings, P.W.; Kern, R.; Reitsma, S.; Toppila-Salmi, S.; Bernal-Sprekelsen, M.; Mullol, J.; Alobid, I.; et al. European Position Paper on Rhinosinusitis and Nasal Polyps 2020. Rhinology 2020, 58 (Suppl. S29), 1–464. [Google Scholar] [CrossRef] [PubMed]
- Glück, U.; Gebbers, J.O. Ingested probiotics reduce nasal colonization with pathogenic bacteria (Staphylococcus aureus, Streptococcus pneumoniae, and beta-hemolytic streptococci). Am. J. Clin. Nutr. 2003, 77, 517–520. [Google Scholar] [CrossRef] [PubMed]
- Habermann, W.; Zimmermann, K.; Skarabis, H.; Kunze, R.; Rusch, V. Reduction of acute recurrence in patients with chronic recurrent hypertrophic sinusitis by treatment with a bacterial immunostimulant (Enterococcus faecalis Bacteriae of human origin. Arzneimittelforschung. 2002, 52, 622–627. (In German) [Google Scholar] [PubMed]
- Mukerji, S.S.; Pynnonen, M.A.; Kim, H.M.; Singer, A.; Tabor, M.; Terrell, J.E. Probiotics as adjunctive treatment for chronic rhinosinusitis: A randomized controlled trial. Otolaryngol. Head Neck Surg. 2009, 140, 202–208. [Google Scholar] [CrossRef] [PubMed]
- Mårtensson, A.; Abolhalaj, M.; Lindstedt, M.; Mårtensson, A.; Olofsson, T.C.; Vásquez, A.; Greiff, L.; Cervin, A. Clinical efficacy of a topical lactic acid bacterial microbiome in chronic rhinosinusitis: A randomized controlled trial. Laryngoscope Investig. Otolaryngol. 2017, 2, 410–416. [Google Scholar] [CrossRef] [PubMed]
- Endam, L.M.; Alromaih, S.; Gonzalez, E.; Madrenas, J.; Cousineau, B.; Renteria, A.E.; Desrosiers, M. Intranasal Application of Lactococcus lactis W136 Is Safe in Chronic Rhinosinusitis Patients With Previous Sinus Surgery. Front. Cell. Infect. Microbiol. 2020, 10, 440. [Google Scholar] [CrossRef] [PubMed]
- De Boeck, I.; van den Broek, M.F.L.; Allonsius, C.N.; Spacova, I.; Wittouck, S.; Martens, K.; Wuyts, S.; Cauwenberghs, E.; Jokicevic, K.; Vandenheuvel, D.; et al. Lactobacilli Have a Niche in the Human Nose. Cell Rep. 2020, 31, 107674. [Google Scholar] [CrossRef] [PubMed]
- Babu, H.; Sharma, R.; Sharma, V.K.; Goyal, R.; Rana, A.K. Does FESS alter the sinonasal microbiome. Egypt. J. Ear Nose Throat Allied Sci. 2022, 23, 1–6. [Google Scholar] [CrossRef]
- Hauser, L.J.; Ir, D.; Kingdom, T.T.; Robertson, C.E.; Frank, D.N.; Ramakrishnan, V.R. Investigation of bacterial repopulation after sinus surgery and perioperative antibiotics. Int. Forum. Allergy Rhinol. 2016, 6, 34–40. [Google Scholar] [CrossRef] [PubMed]
- Jain, R.; Hoggard, M.; Biswas, K.; Zoing, M.; Jiang, Y.; Douglas, R. Changes in the bacterial microbiome of patients with chronic rhinosinusitis after endoscopic sinus surgery. Int. Forum. Allergy Rhinol. 2017, 7, 7–15. [Google Scholar] [CrossRef] [PubMed]
- Kidd, P. Th1/Th2 balance: The hypothesis, its limitations, and implications for health and disease. Altern. Med. Rev. 2003, 8, 223–246. [Google Scholar] [PubMed]
- John, D.; Michael, D.; Dabcheva, M.; Hulme, E.; Illanes, J.; Webberley, T.; Wang, D.; Plummer, S. A double-blind, randomized, placebo-controlled study assessing the impact of probiotic supplementation on antibiotic induced changes in the gut microbiome. Front. Microbiomes. 2024, 3, 1359580. [Google Scholar]
- Li, X.; Wang, Q.; Hu, X.; Liu, W. Current Status of Probiotics as Supplements in the Prevention and Treatment of Infectious Diseases. Front. Cell. Infect. Microbiol. 2022, 12, 789063. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Dong, B.R.; Hao, Q. Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Syst. Rev. 2022, 8, CD006895. [Google Scholar] [CrossRef] [PubMed]
Variable | n | Min | Max | Median | Q1 | Q3 | Mean | SD |
---|---|---|---|---|---|---|---|---|
Age | 425 | 19 | 84 | 47 | 37 | 61 | 48.878 | 14.928 |
Duration of symptoms (years) | 344 | 0 | 50 | 4 | 2 | 10 | 6.464 | 7.058 |
Lund–Mackay score | 364 | 1 | 24 | 11 | 8 | 16 | 11.742 | 5.39 |
VAS nasal discharge before ESS | 356 | 0 | 10 | 5.25 | 4 | 8 | 5.625 | 2.764 |
VAS nasal obstruction before ESS | 356 | 0 | 10 | 7 | 4 | 8.5 | 6.296 | 2.758 |
VAS headache before ESS | 356 | 0 | 10 | 4 | 1 | 7 | 4.048 | 3.254 |
VAS smell before ESS | 356 | 0 | 10 | 4 | 0.5 | 9 | 4.688 | 3.988 |
SNOT-22 score before ESS | 353 | 0 | 108 | 46 | 30 | 60 | 45.742 | 19.811 |
VAS nasal discharge after ESS | 297 | 0 | 10 | 3 | 1 | 5 | 3.458 | 2.618 |
VAS nasal obstruction after ESS | 297 | 0 | 10 | 2 | 0 | 5 | 2.798 | 2.766 |
VAS headache after ESS | 297 | 0 | 10 | 1 | 0 | 4 | 2.392 | 2.717 |
VAS smell after ESS | 297 | 0 | 10 | 2 | 0 | 7 | 3.621 | 3.632 |
SNOT-22 score after ESS | 295 | 0 | 85 | 24 | 12 | 40.5 | 28.112 | 19.995 |
Variable | No Synbiotic n = 231 (100%) 1 | Synbiotic n = 194 (100%) 1 | p2 |
---|---|---|---|
Sex | 0.003 | ||
Male | 144 (62%) | 92 (47%) | |
Female | 87 (38%) | 102 (53%) | |
Presence of nasal discharge | 195 (86%) | 167 (86%) | >0.99 |
Nasal obstruction | 198 (87%) | 171 (88%) | 0.89 |
Headaches | 129 (57%) | 135 (75%) | 0.008 |
Olfactory disturbances | 130 (57%) | 106 (55%) | 0.66 |
Previous sinus surgeries: | 0.58 | ||
None | 132 (58%) | 126 (65%) | |
One | 58 (25%) | 43 (22%) | |
More than one | 38 (17%) | 25 (13%) | |
Hypertension | 72 (31%) | 53 (27%) | 0.43 |
Diabetes mellitus | 9 (4%) | 10 (5%) | 0.70 |
Asthma | 51 (22%) | 46 (24%) | 0.80 |
Inhalant allergy | 70 (30%) | 66 (34%) | 0.49 |
NSAID hypersensitivity | 28(12%) | 20 (10%) | 0.65 |
Smoking | 64 (28%) | 44 (23%) | 0.27 |
Occupational exposure to harmful agents | 36 (16%) | 38 (20%) | 0.35 |
Postoperative antibiotic use | 84 (51%) | 61 (36%) | 0.018 |
Variable | Group | n | Min | Max | Median | Q1 | Q3 | Mean | SD | p |
---|---|---|---|---|---|---|---|---|---|---|
Age | Without synbiotic | 231 | 21 | 80 | 48 | 38.5 | 62.5 | 49.792 | 14.592 | 0.17 |
Synbiotic | 194 | 19 | 84 | 46 | 35 | 60 | 47.789 | 15.286 | ||
Duration of symptoms (in years) | Without synbiotic | 152 | 0 | 40 | 4 | 2 | 8.25 | 6.131 | 6.739 | 0.428 |
Synbiotic | 192 | 0.25 | 50 | 5 | 2 | 10 | 6.727 | 7.308 | ||
Bacterial colony count before ESS | Without synbiotic | 227 | 0 | 4 | 2 | 1 | 3 | 1.89 | 1.245 | 0.58 |
Synbiotic | 192 | 0 | 3 | 3 | 0 | 3 | 1.922 | 1.318 | ||
Bacterial colony count after ESS | Without synbiotic | 181 | 0 | 4 | 1 | 0 | 3 | 1.431 | 1.217 | 0.044 |
Synbiotic | 162 | 0 | 3 | 1 | 0 | 2 | 1.173 | 1.224 |
Variable (Bacteriological Result) | Without Synbiotic n = 231 (100%) 1 | Synbiotic n = 194 (100%) 1 | p 2 |
---|---|---|---|
Swab 1: Acinetobacter lwoffii | 1 (0%) | 1 (1%) | >0.99 |
Swab 1: Aspergillus spp. | 1 (0%) | 1 (1%) | >0.99 |
Swab 1: Bacteroides ovatus | 1 (0%) | 1(1%) | >0.99 |
Swab 1: Candida spp. | 1 (0%) | 2 (1%) | 0.88 |
Swab 1: Corynebacterium acconlens | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Citrobacter freundii | 4 (2%) | 7 (4%) | 0.36 |
Swab 1: Citrobacter koseri | 5 (2%) | 7(4%) | 0.55 |
Swab 1: Enterobacter aerogenes | 3 (1%) | 4 (2%) | 0.82 |
Swab 1: Enterobacter cloacae | 6 (3%) | 3 (2%) | 0.68 |
Swab 1: Enterococcus faecalis | 2 (1%) | 3 (2%) | 0.84 |
Swab 1: Escherichia coli | 37 (16%) | 20 (10%) | 0.11 |
Swab 1: physiological flora | 1 (0%) | 6 (3%) | 0.078 |
Swab 1: Haemophilus influenzae | 5 (2%) | 0 (0%) | 0.11 |
Swab 1: Hafnia alvei | 0 (0%) | 1 (1%) | 0.93 |
Swab 1: Klebsiella aerogenes | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Klebsiella oxytoca | 17 (7%) | 18 (9%) | 0.59 |
Swab 1: Klebsiella pneumoniae | 12 (5%) | 19 (10%) | 0.10 |
Swab 1: Morganella morganii | 4 (2%) | 5 (3%) | 0.79 |
Swab 1: Prevotella oralis | 1 (0%) | 0 (0)% | >0.99 |
Swab 1: Proteus hauseri | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Proteus mirabilis | 9 (4%) | 9 (5%) | 0.89 |
Swab 1: Pseudomonas aeruginosa | 4 (2%) | 5 (3%) | 0.79 |
Swab 1: Raoultella planticola | 2 (1%) | 2 (1%) | >0.99 |
Swab 1: Serratia liquefaciens | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Serratia marcescens | 4 (2%) | 1 (1%) | 0.48 |
Swab 1: Staphylococcus aureus | 59 (26%) | 59 (30%) | 0.31 |
Swab 1: Staphylococcus aureus MSSA | 11 (5%) | 2 (1%) | 0.052 |
Swab 1: Staphylococcus epidermidis | 11 (5%) | 2 (1%) | 0.12 |
Swab 1: Staphylococcus hominis | 1 (0%) | 1 (1%) | >0.99 |
Swab 1: Staphylococcus lugdunensis | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Coagulase-negative Staphylococcus spp. | 14 (6%) | 0 (0%) | 0.001 |
Swab 1: Stenotrophomonas maltophilia | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Streptococcus agalactiae | 2 (1%) | 0 (0%) | 0.56 |
Swab 1: Group B beta-hemolytic Streptococcus | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Streptococcus canis | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Streptococcus viridans | 1 (0%) | 0 (0%) | >0.99 |
Swab 1: Streptococcus pneumoniae | 3 (1%) | 0 (0%) | 0.31 |
Swab 1: Streptococcus pyogenes | 1 (0%) | 1 (1%) | >0.99 |
Swab 1: negative | 50 (22%) | 44 (23%) | 0.89 |
Swab 1: saprophytic cocci | 0 (0%) | 1 (1%) | 0.93 |
Swab 2: Acinetobacter baumannii | 3 (1%) | 2 (1%) | >0.99 |
Swab 2: Acinetobacter lwoffii | 0 (0%) | 1 (1%) | 0.93 |
Swab 2: Acinetobacter ursingii | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Candida spp. | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Citrobacter freundii | 1 (0%) | 3 (2%) | 0.50 |
Swab 2: Citrobacter koseri | 3 (1%) | 3 (2%) | >0.99 |
Swab 2: Citrobakter braakii | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Corynebacterium accolens | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Corynebacterium pseudodiphtheriticum | 3 (1%) | 0 (0%) | 0.31 |
Swab 2: Enterobacter cloacae | 2 (1%) | 5 (3%) | 0.32 |
Swab 2: Enterococcus faecalis | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Escherichia coli | 15 (6%) | 8 (4%) | 0.39 |
Swab 2: physiological flora | 16 (7%) | 22 (11%) | 0.16 |
Swab 2: Haemophilus influenzae | 5 (2%) | 1 (1%) | 0.31 |
Swab 2: Klebsiella oxytoca | 4 (2%) | 9 (5%) | 0.15 |
Swab 2: Klebsiella pneumoniae | 7 (3%) | 6 (3%) | >0.99 |
Swab 2: Moraxella catarhalis | 0 (0%) | 1 (1%) | 0.93 |
Swab 2: Moraxella nonliquefaciens | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Morganella morganii | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Pantoea spp. | 2 (1%) | 0 (0%) | 0.56 |
Swab 2: Proteus mirabilis | 7 (3%) | 2 (1%) | 0.28 |
Swab 2: Pseudomonas aeruginosa | 2 (1%) | 4 (2%) | 0.53 |
Swab 2: Pseudomonas luteola | 0 (0%) | 1 (1%) | 0.93 |
Swab 2: Raoultella ornithinolytica | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Raoultella planticola | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Serratia marcescens | 4 (2%) | 2 (1%) | 0.84 |
Swab 2: Staphylococcus aureus | 50 (22%) | 53 (27%) | 0.18 |
Swab 2: Staphylococcus aureus MSSA | 12 (5%) | 3 (2%) | 0.077 |
Swab 2: Coagulase-negative Staphylococcus spp. | 24 (10%) | 0 (0%) | <0.001 |
Swab 2: Streptococcus constellatus | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Streptococcus viridans | 1 (0%) | 0 (0%) | >0.99 |
Swab 2: Streptococcus pneumoniae | 6 (3%) | 3 (2%) | 0.68 |
Swab 2: negative | 41 (18%) | 46 (24%) | 0.16 |
Variable (Bacteriological Result) | Without Synbiotic n = 78 1 | Synbiotic n = 107 1 | p 2 |
---|---|---|---|
Swab 1: Candida albicans | 1 (1%) | 2 (2%) | >0.99 |
Swab 1: Citrobacter freundii | 0 (0%) | 5 (5%) | 0.14 |
Swab 1: Citrobacter koseri | 1 (1%) | 3 (3%) | 0.85 |
Swab 1: Enterobacter aerogenes | 1 (1%) | 2 (2%) | >0.99 |
Swab 1: Enterobacter cloacae | 2 (3%) | 2 (2%) | >0.99 |
Swab 1: Enterococcus faecalis | 0 (0%) | 2 (2%) | 0.62 |
Swab 1: Escherichia coli | 9 (12%) | 2 (2%) | 0.015 |
Swab 1: physiological flora | 1 (1%) | 2 (2%) | >0.99 |
Swab 1: Hafnia alvei | 0 (0%) | 1 (1%) | >0.99 |
Swab 1: Klebsiella oxytoca | 4 (5%) | 8 (7%) | 0.74 |
Swab 1: Klebsiella pneumoniae | 2 (3%) | 8 (7%) | 0.26 |
Swab 1: Morganella morganii | 1 (1%) | 3 (3%) | 0.85 |
Swab 1: Prevotella oralis | 1 (1%) | 0 (0%) | 0.87 |
Swab 1: Proteus mirabilis | 3 (4%) | 3 (3%) | >0.99 |
Swab 1: Pseudomonas aeruginosa | 1 (1%) | 4 (4%) | 0.58 |
Swab 1: Raoultella planticola | 0 (0%) | 1 (1%) | >0.99 |
Swab 1: Serratia marcescens | 0 (0%) | 1 (1%) | >0.99 |
Swab 1: Staphylococcus aureus | 9 (12%) | 34 (32%) | 0.002 |
Swab 1: Staphylococcus aureus MSSA | 6 (8%) | 1 (1%) | 0.047 |
Swab 1: Staphylococcus epidermidis | 5 (6%) | 1 (1%) | 0.40 |
Swab 1: Staphylococcus lugdunensis | 1 (1%) | 0 (0%) | 0.87 |
Swab 1: Stenotrophomonas maltophilia | 1 (1%) | 0 (0%) | 0.87 |
Swab 1: Streptococcus pyogenes | 1 (1%) | 1 (1%) | >0.99 |
Swab 1: negative | 34 (44%) | 35 (33%) | 0.17 |
Swab 1: saprophytic cocci | 0 (0%) | 1 (1%) | >0.99 |
Swab 2: Acinetobacter baumannii | 0 (0%) | 1 (1%) | >0.99 |
Swab 2: Acinetobacter lwoffii | 0 (0%) | 1 (1%) | >0.99 |
Swab 2: Citrobacter freundii | 1 (1%) | 3 (3%) | 0.85 |
Swab 2: Citrobacter koseri | 1 (1%) | 3 (3%) | 0.85 |
Swab 2: Enterobacter cloacae | 2 (3%) | 4 (4%) | 0.98 |
Swab 2: Escherichia coli | 3 (4%) | 2 (2%) | 0.72 |
Swab 2: physiological flora | 10 (13%) | 14 (13%) | >0.99 |
Swab 2: Haemophilus influenzae | 2 (3%) | 1 (1%) | 0.78 |
Swab 2: Klebsiella oxytoca | 1 (1%) | 6 (6%) | 0.26 |
Swab 2: Klebsiella pneumoniae | 1 (1%) | 6 (6%) | 0.26 |
Swab 2: Moraxella catarhalis | 0 (0%) | 1 (1%) | >0.99 |
Swab 2: Pantoea spp. | 1 (1%) | 0 (0%) | 0.87 |
Swab 2: Proteus mirabilis | 1 (1%) | 2 (2%) | >0.99 |
Swab 2: Pseudomonas aeruginosa | 0 (0%) | 3 (3%) | 0.37 |
Swab 2: Raoultella planticola | 1 (1%) | 0 (0%) | 0.87 |
Swab 2: Serratia marcescens | 1 (1%) | 2 (2%) | >0.99 |
Swab 2: Staphylococcus aureus | 19 (24%) | 33 (31%) | 0.42 |
Swab 2: Staphylococcus aureus MSSA | 8 (10%) | 2 (2%) | 0.17 |
Swab 2: Streptococcus pneumoniae | 0 (0%) | 2 (2%) | 0.62 |
Swab 2: negative | 25 (32%) | 25 (23%) | 0.25 |
Without Synbiotic | Synbiotic | |||||
---|---|---|---|---|---|---|
Variable (Bacteriological Result) | Before n = 231 1 | After n = 231 1 | p 2 | Before n = 194 1 | After n = 194 1 | p 2 |
Acinetobacter baumannii | 0 (0%) | 3 (1%) | 0.25 | 0 (0%) | 2 (1%) | 0.48 |
Acinetobacter lwoffii | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 1 (1%) | >0.99 |
Acinetobacter ursingii | 0 (0%) | 1 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Aspergillus spp. | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Bacteroides ovatus | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Candida albicans | 1 (0%) | 0 (0%) | >0.99 | 2 (1%) | 0 (0%) | 0.48 |
Candida spp. | 0 (0%) | 1 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Corynebacterium acconlens | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Citrobacter freundii | 4 (2%) | 1 (0%) | 0.37 | 7 (4%) | 3 (2%) | 0.34 |
Citrobacter koseri | 5 (2%) | 3 (1%) | 0.72 | 7 (4%) | 3 (2%) | 0.34 |
Citrobakter brakii | 0 (0%) | 1 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Corynebacterium accolens | 0 (0%) | 1 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Corynebacterium pseudodiphtheriticum | 0 (0%) | 3 (1%) | 0.25 | 0 (0%) | 0 (0%) | |
Enterobacter aerogenes | 3 (1%) | 0 (0%) | 0.25 | 4 (2%) | 0 (0%) | 0.13 |
Enterobacter cloacae | 6 (3%) | 2 (1%) | 0.28 | 3 (2%) | 5 (3%) | 0.72 |
Enterococcus faecalis | 2 (1%) | 1 (0%) | >0.99 | 3 (2%) | 0 (0%) | 0.25 |
Escherichia coli | 37 (16%) | 15 (6%) | 0.002 | 20 (10%) | 8 (4%) | 0.031 |
Physiological flora | 1 (0%) | 16 (7%) | <0.001 | 6 (3%) | 22 (11%) | 0.003 |
Haemophilus influenzae | 5 (2%) | 5 (2%) | >0.99 | 0 (0%) | 1 (1%) | >0.99 |
Hafnia alvei | 0 (0%) | 0 (0%) | 1 (1%) | 0 (0%) | >0.99 | |
Klebsiella aerogenes | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Klebsiella oxytoca | 17 (7%) | 4 (2%) | 0.007 | 18 (9%) | 9 (5%) | 0.11 |
Klebsiella pneumoniae | 12 (5%) | 7 (3%) | 0.35 | 19 (10%) | 6 (3%) | 0.013 |
Moraxella catarhalis | 0 (0%) | 0 (0%) | 0 (0%) | 1 (1%) | >0.99 | |
Moraxella nonliquefaciens | 0 (0%) | 1 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Morganella morganii | 4 (2%) | 1 (0%) | 0.37 | 5 (3%) | 0 (0%) | 0.072 |
Pantoea spp. | 0 (0%) | 2 (1%) | 0.48 | 0 (0%) | 0 (0%) | |
Prevotella oralis | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Proteus hauseri | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Proteus mirabilis | 9 (4%) | 7 (3%) | 0.80 | 9 (5%) | 2 (1%) | 0.066 |
Pseudomonas aeruginosa | 4 (2%) | 2 (1%) | 0.68 | 5 (3%) | 4 (2%) | >0.99 |
Pseudomonas luteola | 0 (0%) | 0 (0%) | 0 (0%) | 1 (1%) | >0.99 | |
Raoultella ornithinolytica | 0 (0%) | 1 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Raoultella planticola | 2 (1%) | 1 (0%) | >0.99 | 2 (1%) | 0 (0%) | 0.48 |
Serratia liquefaciens | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Serratia marcescens | 4 (2%) | 4 (2%) | >0.99 | 1 (1%) | 2 (1%) | >0.99 |
Staphylococcus aureus | 59 (26%) | 50 (22%) | 0.38 | 59 (30%) | 53 (27%) | 0.58 |
Staphylococcus aureus MSSA | 11 (5%) | 12 (5%) | >0.99 | 2 (1%) | 3 (2%) | >0.99 |
Staphylococcus epidermidis | 11 (5%) | 0 (0%) | 0.002 | 2 (1%) | 0 (0%) | 0.48 |
Staphylococcus hominis | 1 (0%) | 0 (0%) | >0.99 | 1 (1%) | 0 (0%) | >0.99 |
Staphylococcus lugdunensis | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Coagulase-negative Staphylococcus spp. | 14 (6%) | 24 (10%) | 0.13 | 0 (0%) | 0 (0%) | |
Stenotrophomonas maltophilia | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Streptococcus constellatus | 0 (0%) | 1 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Streptococcus agalactiae | 2 (1%) | 0 (0%) | 0.48 | 0 (0%) | 0 (0%) | |
Group B beta-hemolytic Streptococcus | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Streptococcus canis | 1 (0%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Streptococcus viridans | 1 (0%) | 1 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Streptococcus pneumoniae | 3 (1%) | 6 (3%) | 0.50 | 0 (0%) | 3 (2%) | 0.25 |
Streptococcus pyogenes | 1 (0%) | 0 (0%) | >0.99 | 1 (1%) | 0 (0%) | >0.99 |
Negative swab | 50 (22%) | 41 (18%) | 0.35 | 44 (23%) | 46 (24%) | 0.90 |
Saprophytic cocci | 0 (0%) | 0 (0%) | 1 (1%) | 0 (0%) | >0.99 | |
Type of bacteria | 0.001 | 0.038 | ||||
Gram-positive bacteria | 73 (41%) | 77 (62%) | 49 (35%) | 48 (52%) | ||
Gram-negative bacteria | 75 (43%) | 31 (25%) | 74 (53%) | 35 (38%) | ||
Gram-positive and Gram-negative bacteria | 28 (16%) | 16 (13%) | 17 (12%) | 10 (11%) |
Without Synbiotic | Synbiotic | |||||
---|---|---|---|---|---|---|
Variable (Bacteriological Result) | Before n = 78 1 | After n = 78 1 | p 2 | Before n = 107 1 | After n = 107 1 | p 2 |
Acinetobacter baumannii | 0 (0%) | 0 (0%) | 0 (0%) | 1 (1%) | >0.99 | |
Acinetobacter lwoffii | 0 (0%) | 0 (0%) | 0 (0%) | 1 (1%) | >0.99 | |
Candida albicans | 1 (1%) | 0 (0%) | >0.99 | 2 (2%) | 0 (0%) | 0.48 |
Citrobacter freundii | 0 (0%) | 1 (1%) | >0.99 | 5 (5%) | 3 (3%) | 0.72 |
Citrobacter koseri | 1 (1%) | 1 (1%) | >0.99 | 3 (3%) | 3 (3%) | >0.99 |
Enterobacter aerogenes | 1 (1%) | 0 (0%) | >0.99 | 2 (2%) | 0 (0%) | 0.48 |
Enterobacter cloacae | 2 (3%) | 2 (3%) | >0.99 | 2 (2%) | 4 (4%) | 0.68 |
Enterococcus faecalis | 0 (0%) | 0 (0%) | 2 (2%) | 0 (0%) | 0.48 | |
Escherichia coli | 9 (12%) | 3 (4%) | 0.13 | 2 (2%) | 2 (2%) | >0.99 |
Physiological flora | 1 (1%) | 10 (13%) | 0.012 | 2 (2%) | 14 (13%) | 0.004 |
Haemophilus influenzae | 0 (0%) | 2 (3%) | 0.48 | 0 (0%) | 1 (1%) | >0.99 |
Hafnia alvei | 0 (0%) | 0 (0%) | 1 (1%) | 0 (0%) | >0.99 | |
Klebsiella oxytoca | 4 (5%) | 1 (1%) | 0.36 | 8 (7%) | 6 (6%) | 0.78 |
Klebsiella pneumoniae | 2 (3%) | 1 (1%) | >0.99 | 8 (7%) | 6 (6%) | 0.78 |
Moraxella catarhalis | 0 (0%) | 0 (0%) | 0 (0%) | 1 (1%) | >0.99 | |
Morganella morganii | 1 (1%) | 0 (0%) | >0.99 | 3 (3%) | 0 (0%) | 0.24 |
Pantoea spp. | 0 (0%) | 1 (1%) | >0.99 | 0 (0%) | 0 (0%) | |
Prevotella oralis | 1 (1%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Proteus mirabilis | 3 (4%) | 1 (1%) | 0.61 | 3 (3%) | 2 (2%) | >0.99 |
Pseudomonas aeruginosa | 1 (1%) | 0 (0%) | >0.99 | 4 (4%) | 3 (3%) | >0.99 |
Raoultella planticola | 0 (0%) | 1 (1%) | >0.99 | 1 (1%) | 0 (0%) | >0.99 |
Serratia marcescens | 0 (0%) | 1 (1%) | >0.99 | 1 (1%) | 2 (2%) | >0.99 |
Staphylococcus aureus | 9 (12%) | 19 (24%) | 0.060 | 34 (32%) | 33 (31%) | >0.99 |
Staphylococcus aureus MSSA | 6 (8%) | 8 (10%) | 0.78 | 1 (1%) | 2 (2%) | >0.99 |
Staphylococcus epidermidis | 5 (6%) | 0 (0%) | 0.069 | 1 (1%) | 0 (0%) | >0.99 |
Staphylococcus lugdunensis | 1 (1%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Stenotrophomonas maltophilia | 1 (1%) | 0 (0%) | >0.99 | 0 (0%) | 0 (0%) | |
Streptococcus pneumoniae | 0 (0%) | 0 (0%) | 0 (0%) | 2 (2%) | 0.48 | |
Streptococcus pyogenes | 1 (1%) | 0 (0%) | >0.99 | 1 (1%) | 0 (0%) | >0.99 |
Negative swab | 34 (44%) | 25 (32%) | 0.19 | 35 (33%) | 25 (23%) | 0.17 |
saprophytic cocci | 0 (0%) | 0 (0%) | 1 (1%) | 0 (0%) | >0.99 | |
Type of bacteria | 0.16 | 0.70 | ||||
Gram-positive bacteria | 18 (43%) | 23 (62%) | 28 (42%) | 30 (48%) | ||
Gram-negative bacteria | 20 (48%) | 10 (27%) | 29 (44%) | 26 (42%) | ||
Gram-positive and Gram-negative bacteria | 4 (10%) | 4 (11%) | 9 (14%) | 6 (10%) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Published by MDPI on behalf of the Lithuanian University of Health Sciences. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Goroszkiewicz, K.; Lisowska, G.; Stryjewska-Makuch, G.; Karłowska-Bijak, O.; Misiołek, M. The Impact of Synbiotics on the Bacterial Flora During the Course of Chronic Sinusitis. Medicina 2025, 61, 1306. https://doi.org/10.3390/medicina61071306
Goroszkiewicz K, Lisowska G, Stryjewska-Makuch G, Karłowska-Bijak O, Misiołek M. The Impact of Synbiotics on the Bacterial Flora During the Course of Chronic Sinusitis. Medicina. 2025; 61(7):1306. https://doi.org/10.3390/medicina61071306
Chicago/Turabian StyleGoroszkiewicz, Karolina, Grażyna Lisowska, Grażyna Stryjewska-Makuch, Olga Karłowska-Bijak, and Maciej Misiołek. 2025. "The Impact of Synbiotics on the Bacterial Flora During the Course of Chronic Sinusitis" Medicina 61, no. 7: 1306. https://doi.org/10.3390/medicina61071306
APA StyleGoroszkiewicz, K., Lisowska, G., Stryjewska-Makuch, G., Karłowska-Bijak, O., & Misiołek, M. (2025). The Impact of Synbiotics on the Bacterial Flora During the Course of Chronic Sinusitis. Medicina, 61(7), 1306. https://doi.org/10.3390/medicina61071306