Analysis of Bacterial Biofilm Formation and MUC5AC and MUC5B Expression in Chronic Rhinosinusitis Patients
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design, Patients and Tissue Collection
2.2. Bacterial Biofilm Identification
2.2.1. Sample Staining and Image Acquisition
2.2.2. Biofilm Criteria
2.3. MUC5AC and MUC5B Expression Level Quantification
2.4. Statistical Analysis
3. Results
3.1. Patient Demographics
3.2. Evaluation of Bacterial Biofilm Status
3.3. Evaluation of MUC5AC and MUC5B Expression Levels
3.4. Investigating the Possible Relationship between Bacterial Biofilm Formation and Mucin Expression Levels
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Halawi, A.M.; Smith, S.S.; Chandra, R.K. Chronic rhinosinusitis: Epidemiology and cost. Allergy Asthma Proc. 2013, 34, 328–334. [Google Scholar] [CrossRef] [PubMed]
- DeConde, A.S.; Soler, Z.M. Chronic rhinosinusitis: Epidemiology and burden of disease. Am. J. Rhinol. Allergy 2016, 30, 134–139. [Google Scholar] [CrossRef] [PubMed]
- Hastan, D.; Fokkens, W.J.; Bachert, C.; Newson, R.B.; Bislimovska, J.; Bockelbrink, A.; Bousquet, P.J.; Brozek, G.; Bruno, A.; Dahlén, S.E.; et al. Chronic rhinosinusitis in Europe—An underestimated disease. A GA 2LEN study. Allergy Eur. J. Allergy Clin. Immunol. 2011, 66, 1216–1223. [Google Scholar] [CrossRef] [PubMed]
- Rudmik, L.; Smith, T.L. Quality of life in patients with chronic rhinosinusitis. Curr. Allergy Asthma Rep. 2011, 11, 247–252. [Google Scholar] [CrossRef] [PubMed]
- Rudmik, L. Economics of Chronic Rhinosinusitis. Curr. Allergy Asthma Rep. 2017, 17, 20. [Google Scholar] [CrossRef] [PubMed]
- Rosenfeld, S.; Piccirillo, R.M.; Chandrasekhar, J.F. Diagnostic Criteria for Rhinosinusitis. Clin. Pract. Guidel. Am. Acad. Otolaryngol. Neck Surg. 2015, 152, S1–S39. [Google Scholar]
- Hamilos, D.L. Chronic rhinosinusitis: Epidemiology and medical management. J. Allergy Clin. Immunol. 2011, 128, 693–707. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, S.; Sharma, R.; Sharma, V.K.; Rana, A.K. Effect of Functional Endoscopic Sinus Surgery on Mucociliary Clearance in Patients of Chronic Rhinosinusitis. Otorhinolaryngol. Clin. 2021, 13, 37–39. [Google Scholar]
- Cain, R.B.; Lal, D. Update on the management of chronic rhinosinusitis. Infect. Drug Resist. 2013, 6, 1–14. [Google Scholar]
- Foreman, A.; Boase, S.; Psaltis, A.; Wormald, P.J. Role of bacterial and fungal biofilms in chronic rhinosinusitis. Curr. Allergy Asthma Rep. 2012, 12, 127–135. [Google Scholar] [CrossRef]
- Bjarnsholt, T.; Tolker-Nielsen, T.; Givskov, M.; Janssen, M.; Christensen, L.H. Detection of bacteria by fluorescence in situ hybridization in culture-negative soft tissue filler lesions. Dermatol. Surg. 2009, 35 (Suppl. 2), 1620–1624. [Google Scholar] [CrossRef] [PubMed]
- Gok, U.; Bulut, Y.; Keles, E.; Yalcin, S.; Doymaz, M.Z. Bacteriological and PCR analysis of clinical material aspirated from otitis media with effusions. Int. J. Pediatr. Otorhinolaryngol. 2001, 60, 49–54. [Google Scholar] [CrossRef] [PubMed]
- Rayner, M.G.; Zhang, Y.; Gorry, M.C.; Chen, Y.; Post, J.C.; Ehrlich, G.D. Evidence of bacterial metabolic activity in culture-negative otitis media with effusion. J. Am. Med. Assoc. 1998, 279, 296–299. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parsa, K.; Schaudinn, C.; Gorur, A.; Sedghizadeh, P.P.; Johnson, T.; Tse, D.T.; Costerton, J.W. Demonstration of bacterial biofilms in culture-negative silicone stent and jones tube. Ophthal. Plast. Reconstr. Surg. 2010, 26, 426–430. [Google Scholar] [CrossRef]
- Hall-Stoodley, L.; Hu, F.Z.; Gieseke, A.; Nistico, L.; Nguyen, D.; Hayes, J.; Forbes, M.; Greenberg, D.P.; Dice, B.; Burrows, A.; et al. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. J. Am. Med. Assoc. 2006, 296, 202–211. [Google Scholar] [CrossRef] [Green Version]
- Sanderson, A.R.; Leid, J.G.; Hunsaker, D. Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis. Laryngoscope 2006, 116, 1121–1126. [Google Scholar] [CrossRef]
- Sanclement, J.A.; Webster, P.; Thomas, J.; Ramadan, H.H. Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis. Laryngoscope 2005, 115, 578–582. [Google Scholar] [CrossRef]
- Psaltis, A.J.; Ha, K.R.; Beule, A.G.; Tan, L.W.; Wormald, P.J. Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope 2007, 117, 1302–1306. [Google Scholar] [CrossRef]
- Li, H.; Wang, D.; Sun, X.; Hu, L.; Yu, H.; Wang, J. Relationship between bacterial biofilm and clinical features of patients with chronic rhinosinusitis. Eur. Arch. Oto-Rhino-Laryngol. 2012, 269, 155–163. [Google Scholar] [CrossRef]
- Psaltis, A.J.; Weitzel, E.K.; Ha, K.R.; Wormald, P.J. The effect of bacterial biofilms on post-sinus surgical outcomes. Am. J. Rhinol 2008, 22, 1–6. [Google Scholar] [CrossRef]
- Głowacki, R.; Tomaszewski, K.A.; Str, P.; Tomaszewska, I.M.; Zgórska-Świerzy, K.; Markiewicz, B.; Składzień, J. The influence of bacterial biofilm on the clinical outcome of chronic rhinosinusitis: A prospective, double-blind, scanning electron microscopy study. Eur. Arch. Oto-Rhino-Laryngol. 2014, 271, 1015–1021. [Google Scholar] [CrossRef] [PubMed]
- Hänsch, G.M. Host Defence against Bacterial Biofilms: ‘Mission Impossible’? ISRN Immunol. 2012, 2012, 853123. [Google Scholar] [CrossRef] [Green Version]
- Dufour, D.; Leung, V.; Lévesque, C.M. Bacterial biofilm: Structure, function, and antimicrobial resistance. Endod. Top. 2010, 22, 2–16. [Google Scholar] [CrossRef]
- Fastenberg, J.H.; Hsueh, W.D.; Mustafa, A.; Akbar, N.A.; Abuzeid, W.M. Biofilms in chronic rhinosinusitis: Pathophysiology and therapeutic strategies. World J. Otorhinolaryngol.-Head Neck Surg. 2016, 2, 219–229. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ramakrishnan, Y.; Shields, R.C.; ElBadawey, M.R.; Wilson, J.A. Biofilms in chronic rhinosinusitis: What is new and where next? J. Laryngol. Otol. 2015, 129, 744–751. [Google Scholar] [CrossRef]
- Kostakioti, M.; Hadjifrangiskou, M.; Hultgren, S.J. Bacterial biofilms: Development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb. Perspect. Med. 2013, 3. [Google Scholar] [CrossRef] [Green Version]
- Vlastarakos, P.V.; Nikolopoulos, T.P.; Maragoudakis, P.; Tzagaroulakis, A.; Ferekidis, E. Biofilms in ear, nose, and throat infections: How important are they? Laryngoscope 2007, 117, 668–673. [Google Scholar] [CrossRef]
- Jackson, D.W.; Suzuki, K.; Oakford, L.; Simecka, J.W.; Hart, M.E.; Romeo, T. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 2002, 184, 290–301. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Z.; Kofonow, J.M.; Finkelman, B.S.; Doghramji, L.; Chiu, A.G.; Kennedy, D.W.; Cohen, N.A.; Palmer, J.N. Clinical factors associated with bacterial biofilm formation in chronic rhinosinusitis. Otolaryngol.-Head Neck Surg. 2011, 144, 457–462. [Google Scholar] [CrossRef]
- Hutcherson, J.A.; Scott, D.A.; Bagaitkar, J. Scratching the surface—Tobacco-induced bacterial biofilms. Tob. Induc. Dis. 2015, 13, 1. [Google Scholar] [CrossRef] [Green Version]
- Hussey, S.J.K.; Purves, J.; Allcock, N.; Fernandes, V.E.; Monks, P.S.; Ketley, J.M.; Andrew, P.W.; Morrissey, J.A. Air pollution alters Staphylococcus aureus and Streptococcus pneumoniae biofilms, antibiotic tolerance and colonisation. Environ. Microbiol. 2017, 19, 1868–1880. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mao, Y.J.; Chen, H.H.; Wang, B.; Liu, X.; Xiong, G.Y. Increased expression of MUC5AC and MUC5B promoting bacterial biofilm formation in chronic rhinosinusitis patients. Auris Nasus Larynx 2015, 42, 294–298. [Google Scholar] [CrossRef] [PubMed]
- Tan, L.; Psaltis, A.; Baker, L.M.; McGuckin, M.; Rousseau, K.; Wormald, P.J. Aberrant mucin glycoprotein patterns of chronic rhinosinusitis patients with bacterial biofilms. Am. J. Rhinol. Allergy 2010, 24, 319–324. [Google Scholar] [CrossRef] [PubMed]
- Thornton, D.J.; Rousseau, K.; McGuckin, M.A. Structure and function of the polymeric mucins in airways mucus. Annu. Rev. Physiol. 2008, 70, 459–486. [Google Scholar] [CrossRef]
- Lillehoj, E.P.; Kato, K.; Lu, W.; Kim, K.C. Cellular and Molecular Biology of Airway Mucins; Elsevier: Amsterdam, The Netherlands, 2013. [Google Scholar]
- Ali, M.S.; Pearson, J.P. Upper airway mucin gene expression: A review. Laryngoscope 2007, 117, 932–938. [Google Scholar] [CrossRef]
- Martínez-Antón, A.; DeBolós, C.; Garrido, M.; Roca-Ferrer, J.; Barranco, C.; Alobid, I.; Xaubet, A.; Picado, C.; Mullol, J. Mucin genes have different expression patterns in healthy and diseased upper airway mucosa. Clin. Exp. Allergy 2006, 36, 448–457. [Google Scholar] [CrossRef]
- Ordoñez, C.L.; Khashayar, R.; Wong, H.H.; Ferrando, R.; Wu, R.; Hyde, D.M.; Hotchkiss, J.A.; Zhang, Y.; Novikov, A.; Dolganov, G.; et al. Mild and moderate asthma is associated with airway goblet cell hyperplasia and abnormalities in mucin gene expression. Am. J. Respir. Crit. Care Med. 2001, 163, 517–523. [Google Scholar] [CrossRef]
- Rose, M.C.; Nickola, T.J.; Voynow, J.A. Airway mucus obstruction: Mucin glycoproteins, MUC gene regulation and goblet cell hyperplasia. Am. J. Respir. Cell Mol. Biol. 2001, 25, 533–537. [Google Scholar] [CrossRef] [Green Version]
- Kim, D.H.; Chu, H.S.; Lee, J.Y.; Hwang, S.J.; Lee, S.H.; Lee, H.M. Up-regulation of MUC5AC and MUC5B mucin genes in chronic rhinosinusitis. Arch. Otolaryngol.-Head Neck Surg. 2004, 130, 747–752. [Google Scholar] [CrossRef] [Green Version]
- Guo, Q.D.; Chun, Q.Z. The expression of MUC5AC and MUC5B mucin genes in the mucosa of chronic rhinosinusitis and nasal polyposis. Am. J. Rhinol. 2007, 21, 359–366. [Google Scholar]
- Landry, R.M.; An, D.; Hupp, J.T.; Singh, P.K.; Parsek, M.R. Mucin-Pseudomonas aeruginosa interactions promote biofilm formation and antibiotic resistance. Mol. Microbiol. 2006, 59, 142–151. [Google Scholar] [CrossRef] [PubMed]
- Kennedy, J.L.; Hubbard, M.A.; Huyett, P.; Patrie, J.T.; Borish, L.; Payne, S.C. Sino-nasal Outcome Test (SNOT-22): A predictor of post-surgical improvement in patients with chronic sinusitis. Ann. Allergy Asthma Immunol. 2014, 111, 246–251. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, Q.; Zhang, J.; Wang, H.; Chen, F.; Luo, X.; Miao, B.; Wu, X.; Ma, R.; Luo, X.; Xu, G.; et al. Expression and regulation of transcription factor FoxA2 in chronic rhinosinusitis with and without nasal polyps. Allergy Asthma Immunol. Res. 2015, 7, 458–466. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seshadri, S.; Lu, X.; Purkey, M.R.; Homma, T.; Choi, A.W.; Carter, R.; Suh, L.; Norton, J.; Harris, K.E.; Conley, D.B.; et al. Increased expression of the epithelial anion transporter pendrin/SLC26A4 in nasal polyps of patients with chronic rhinosinusitis. J. Allergy Clin. Immunol. 2015, 136, 1548–1558.e7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fokkens, S.R.W.J.; Lund, V.J.; Hopkins, C.; Hellings, P.W.; Kern, R. International Rhinology Journal European Position Paper on Rhinosinusitis and Nasal Polyps. EPOS 2020, 1, 7–8. [Google Scholar]
- Ou, J.; Drilling, A.; Singhal, D.; Tan, N.C.W.; Wallis-Hill, D.; Vreugde, S.; Psaltis, A.J.; Wormald, P.J. Association of intracellular Staphylococcus aureus with prognosis in chronic rhinosinusitis. Int. Forum Allergy Rhinol. 2016, 6, 792–799. [Google Scholar] [CrossRef] [PubMed]
- Georgalas, C.; Videler, W.; Freling, N.; Fokkens, W. Global Osteitis Scoring Scale and chronic rhinosinusitis: A marker of revision surgery. Clin. Otolaryngol. 2010, 35, 455–461. [Google Scholar] [CrossRef] [PubMed]
- You, H.; Zhuge, P.; Li, D.; Shao, L.; Shi, H.; Du, H. Factors affecting bacterial biofilm expression in chronic rhinosinusitis and the influences on prognosis. Am. J. Otolaryngol.-Head Neck Med. Surg. 2011, 32, 583–590. [Google Scholar] [CrossRef]
- Bachert, C.; Akdis, C.A. Phenotypes and Emerging Endotypes of Chronic Rhinosinusitis. J. Allergy Clin. Immunol. Pract. 2016, 4, 621–628. [Google Scholar] [CrossRef]
- Akdis, C.A.; Bachert, C.; Cingi, C.; Dykewicz, M.S.; Hellings, P.W.; Naclerio, R.M.; Schleimer, R.P.; Ledford, D. Endotypes and phenotypes of chronic rhinosinusitis: A PRACTALL document of the European Academy of Allergy and Clinical Immunology and the American Academy of Allergy, Asthma & Immunology. J. Allergy Clin. Immunol. 2013, 131, 1479–1490. [Google Scholar]
- Yim, M.T.; Orlandi, R.R. Evolving Rhinology: Understanding the Burden of Chronic Rhinosinusitis Today, Tomorrow, and Beyond. Curr. Allergy Asthma Rep. 2020, 20, 3–7. [Google Scholar] [CrossRef] [PubMed]
- Smith, K.A.; Orlandi, R.R.; Rudmik, L. Cost of adult chronic rhinosinusitis: A systematic review. Laryngoscope 2015, 125, 1547–1556. [Google Scholar] [CrossRef] [PubMed]
- Reh, D.D.; Higgins, T.S.; Smith, T.L. Impact of tobacco smoke on chronic rhinosinusitis: A review of the literature. Int. Forum Allergy Rhinol. 2012, 2, 362–369. [Google Scholar] [CrossRef] [PubMed]
- Marcus, S.; DelGaudio, J.M.; Roland, L.T.; Wise, S.K. Chronic Rhinosinusitis: Does Allergy Play a Role? Med. Sci. 2019, 7, 30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marcus, S.; Roland, L.T.; DelGaudio, J.M.; Wise, S.K. The relationship between allergy and chronic rhinosinusitis. Laryngoscope Investig. Otolaryngol. 2019, 4, 13–17. [Google Scholar] [CrossRef] [Green Version]
- Ou, J.; Wang, J.; Xu, Y.; Tao, Z.Z.; Kong, Y.G.; Chen, S.M.; Shi, W.D. Staphylococcus aureus superantigens are associated with chronic rhinosinusitis with nasal polyps: A meta-analysis. Eur. Arch. Otorhinolaryngol. 2014, 271, 2729–2736. [Google Scholar] [CrossRef]
- Xia, W.; Bai, J.; Wu, X.; Wei, Y.; Feng, S.; Li, L.; Zhang, J.; Xiong, G.; Fan, Y.; Shi, J.; et al. Interleukin-17A promotes MUC5AC expression and goblet cell hyperplasia in nasal polyps via the act1-mediated pathway. PLoS ONE 2014, 9, e98915. [Google Scholar] [CrossRef]
- Luo, Q.; Zhang, Z.; Liu, D.; Feng, K.; Jin, X.; Zhang, J. Human neutrophil elastase induces MUC5AC overexpression in chronic rhinosinusitis through tumour necrosis factor-α converting enzyme. Acta Otolaryngol. 2016, 136, 641–648. [Google Scholar] [CrossRef]
- Kim, H.K.; Kook, J.H.; Kang, K.R.; Oh, D.J.; Kim, T.H.; Lee, S.H. Increased expression of hCLCA1 in chronic rhinosinusitis and its contribution to produce MUC5AC. Laryngoscope 2016, 126, E347–E355. [Google Scholar] [CrossRef]
- Du, J.; Ba, L.; Li, B.; Liu, F.; Hu, X.; Zhang, J.; Liu, Y.; Xian, J.; Liu, S.; Li, H. Distinct expression of NK2 homeobox 1 (NKX2-1) and goblet cell hyperplasia in nasal polyps with different endotypes. Int. Forum Allergy Rhinol. 2017, 7, 690–698. [Google Scholar] [CrossRef]
- Berger, G.; Kogan, T.; Ophir, D.; Skutelsky, E.; Pitaro, K. Glycoconjugate expression of sinus mucosa in chronic rhinosinusitis: A lectin histochemical study. Am. J. Rhinol. 2008, 22, 349–355. [Google Scholar] [CrossRef] [PubMed]
- Bai, J.; Miao, B.; Wu, X.; Luo, X.; Ma, R.; Zhang, J.; Li, L.; Shi, J.; Li, H. Enhanced expression of SAM-pointed domain-containing Ets-like factor in chronic rhinosinusitis with nasal polyps. Laryngoscope 2015, 125, E97–E103. [Google Scholar] [CrossRef] [PubMed]
- Ali, M.S.; Hutton, D.A.; Wilson, J.A.; Pearson, J.P. Major secretory mucin expression in chronic sinusitis. Otolaryngol.-Head Neck Surg. 2005, 133, 423–428. [Google Scholar] [CrossRef] [PubMed]
- Jung, H.H.; Lee, J.H.; Kim, Y.T.; Lee, S.D.; Park, J.H. Expression of Mucin Genes in Chronic Ethmoiditis. Am. J. Rhinol. 2000, 14, 163–170. [Google Scholar] [CrossRef]
- Peña, M.T.; Aujla, P.K.; Patel, K.M.; Zalzal, G.H.; Rose, M.C. Immunohistochemical analyses of MUC5AC mucin expression in sinus mucosa of children with sinusitis and controls. Ann. Otol. Rhinol. Laryngol. 2005, 114, 958–965. [Google Scholar] [CrossRef]
- Viswanathan, H.; Brownlee, I.A.; Pearson, J.P.; Carrie, S. MUC5B secretion is up-regulated in sinusitis compared with controls. Am. J. Rhinol. 2006, 20, 554–557. [Google Scholar] [CrossRef]
- Wu, X.; Amorn, M.M.; Aujla, P.K.; Rice, S.; Mimms, R.; Watson, A.M.; Peters-Hall, J.R.; Rose, M.C.; Peña, M.T. Histologic characteristics and mucin immunohistochemistry of cystic fibrosis sinus mucosa. Arch. Otolaryngol.-Head Neck Surg. 2011, 137, 383–389. [Google Scholar] [CrossRef] [Green Version]
- Saieg, A.; Brown, K.J.; Pena, M.T.; Rose, M.C.; Preciado, D. Proteomic analysis of pediatric sinonasal secretions shows increased MUC5B mucin in CRS. Pediatr. Res. 2015, 77, 356–362. [Google Scholar] [CrossRef]
- Martínez-Antón, A.; De Bolós, C.; Alobid, I.; Benítez, P.; Roca-Ferrer, J.; Picado, C.; Mullol, J. Corticosteroid therapy increases membrane-tethered while decreases secreted mucin expression in nasal polyps. Allergy Eur. J. Allergy Clin. Immunol. 2008, 63, 1368–1376. [Google Scholar] [CrossRef]
- Seong, J.K.; Ja, S.K.; Won, J.L.; Kim, H.N.; Park, J.Y.; Kyoung, S.S.; Ji, H.H.; Yoon, J.H. Upregulation of MUC8 and downregulation of MUC5AC by inflammatory mediators in human nasal polyps and cultured nasal epithelium. Acta Otolaryngol. 2002, 122, 401–407. [Google Scholar] [CrossRef]
- Huang, X.-K.; Yuan, L.; Jin, Y.; Peng, L.; Hong, L. Expression of MUC2 and MUC5B in ethmoid sinus mucosa of patients with chronic rhinosinusitis. Sci. Res. Essays 2010, 5, 1690–1696. [Google Scholar]
- Lasser, C.; O’Neil, S.; Sihlbom, C.; Hansson, S.; Lundback, B.; Lotvall, J. The proteome of nasal exosomes in healthy, asthmatic and chronic rhinosinusitis subjects: A quantitative proteomics approach. Eur. J. Allergy Clin. Immunol. 2012, 67, 590. [Google Scholar]
- Al Badaai, Y.; DiFalco, M.R.; Tewfik, M.A.; Samaha, M. Quantitative proteomics of nasal mucus in chronic sinusitis with nasal polyposis. J. Otolaryngol.-Head Neck Surg. 2009, 38, 381–389. [Google Scholar] [PubMed]
- Peña, M.T.; Aujla, P.K.; Zudaire, E.; Watson, A.M.; Przygodzki, R.; Zalzal, G.H.; Rose, M.C. Localization and expression of MUC5B and MUC7 mucins in pediatric sinus mucosa. Ann. Otol. Rhinol. Laryngol. 2007, 116, 389–397. [Google Scholar] [CrossRef] [PubMed]
- Kato, K.; Song, B.H.; Howe, C.L.; Chang, E.H. A Comprehensive Systematic Review of the Association Between Airway Mucins and Chronic Rhinosinusitis. Am. J. Rhinol. Allergy 2019, 33, 433–448. [Google Scholar] [CrossRef]
Mean Age (Years) | Sex (Men/Women) | Smoking | Nasal Polyposis | Therapy with Nasal Steroids * | Allergy | Mean SNOT-22 Score | |
---|---|---|---|---|---|---|---|
CRS group | 47.24 | 44/22 | 26/66 (39.39%) | 48/66 (72.72%) | 41/66 (62.12%) | 18/66 (27.27%) | 41.15 |
Control group | 32.71 | 10/4 | 3/14 (21.42%) | none | none | 3/14 (21.42%) | 10.85 |
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Popov, G.; Aleksandrov, R.; Petkova, V.; Kaneva, R.; Gergova, R.; Kundurzhiev, T.; Popova, D. Analysis of Bacterial Biofilm Formation and MUC5AC and MUC5B Expression in Chronic Rhinosinusitis Patients. J. Clin. Med. 2023, 12, 1808. https://doi.org/10.3390/jcm12051808
Popov G, Aleksandrov R, Petkova V, Kaneva R, Gergova R, Kundurzhiev T, Popova D. Analysis of Bacterial Biofilm Formation and MUC5AC and MUC5B Expression in Chronic Rhinosinusitis Patients. Journal of Clinical Medicine. 2023; 12(5):1808. https://doi.org/10.3390/jcm12051808
Chicago/Turabian StylePopov, Georgi, Radoslav Aleksandrov, Veronika Petkova, Radka Kaneva, Raina Gergova, Todor Kundurzhiev, and Diana Popova. 2023. "Analysis of Bacterial Biofilm Formation and MUC5AC and MUC5B Expression in Chronic Rhinosinusitis Patients" Journal of Clinical Medicine 12, no. 5: 1808. https://doi.org/10.3390/jcm12051808
APA StylePopov, G., Aleksandrov, R., Petkova, V., Kaneva, R., Gergova, R., Kundurzhiev, T., & Popova, D. (2023). Analysis of Bacterial Biofilm Formation and MUC5AC and MUC5B Expression in Chronic Rhinosinusitis Patients. Journal of Clinical Medicine, 12(5), 1808. https://doi.org/10.3390/jcm12051808