Can Phage Therapy Solve the Problem of Recalcitrant Chronic Rhinosinusitis?

References

• Kern RC , ConleyDB, WalshWet al. Perspectives on the etiology of chronic rhinosinusitis: an immune barrier hypothesis. Am. J. Rhinol. 22 (6), 549 – 559 (2008).
   PubMedGoogle Scholar
• Ghogomu N , KernR. Chronic rhinosinusitis: the rationale for current treatments.Expert Rev. Clin. Immunol.13 (3), 259 – 270 (2017).
   PubMed Web of Science ®Google Scholar
• Fokkens WJ , LundVJ, MullolJet al. European position paper on rhinosinusitis and nasal polyps 2012. Rhinol. Suppl. 3, 1 – 298 (2012).
   Google Scholar
• Gliklich RE , MetsonR. The health impact of chronic sinusitis in patients seeking otolaryngologic care.Otolaryngol. Head Neck Surg.113 (1), 104 – 109 (1995).
   PubMed Web of Science ®Google Scholar
• Miedzybrodzki R , BorysowskiJ, Weber-DabrowskaBet al. Clinical aspects of phage therapy. Adv. Virus Res. 83, 73 – 121 (2012).
   PubMed Web of Science ®Google Scholar
• Gorski A , MiedzybrodzkiR, Weber-DabrowskaBet al. Phage therapy: combating infections with potential for evolving from merely a treatment for complications to targeting diseases. Front. Microbiol. 7, 1515 (2016).
   PubMed Web of Science ®Google Scholar
• Abedon ST , KuhlSJ, BlasdelBG, KutterEM. Phage treatment of human infections.Bacteriophage1 (2), 66 – 85 (2011).
   PubMedGoogle Scholar
• Kutter EM , KuhlSJ, AbedonST. Re-establishing a place for phage therapy in western medicine.Future Microbiol.10 (5), 685 – 688 (2015).
   PubMed Web of Science ®Google Scholar
• Ramakrishnan VR , HauserLJ, FrankDN. The sinonasal bacterial microbiome in health and disease.Curr. Opin. Otolaryngol. Head Neck Surg.24 (1), 20 – 25 (2016).
   PubMed Web of Science ®Google Scholar
• Anderson M , StokkenJ, SanfordT, AuroraR, SindwaniR. A systematic review of the sinonasal microbiome in chronic rhinosinusitis.Am. J. Rhinol. Allergy30 (3), 161 – 166 (2016).
   PubMed Web of Science ®Google Scholar
• Brook I . Microbiology of chronic rhinosinusitis.Eur. J. Clin. Microbiol. Infect. Dis.35 (7), 1059 – 1068 (2016).
   PubMed Web of Science ®Google Scholar
• Ponikau JU , SherrisDA, KernEBet al. The diagnosis and incidence of allergic fungal sinusitis. Mayo Clin. Proc. 74 (9), 877 – 884 (1999).
   PubMed Web of Science ®Google Scholar
• Fokkens WJ , Van DrunenC, GeorgalasC, EbbensF. Role of fungi in pathogenesis of chronic rhinosinusitis: the hypothesis rejected.Curr. Opin. Otolaryngol. Head Neck Surg.20 (1), 19 – 23 (2012).
   PubMed Web of Science ®Google Scholar
• Lanza DC , DhongHJ, TantilipikornP, TanabodeeJ, NadelDM, KennedyDW. Fungus and chronic rhinosinusitis: from bench to clinical understanding.Ann. Otol. Rhinol. Laryngol.115 (9), 27 – 34 (2006).
   Web of Science ®Google Scholar
• Carr TF , HillJL, ChiuA, ChangEH. Alteration in bacterial culture after treatment with topical mupirocin for recalcitrant chronic rhinosinusitis.JAMA Otolaryngol. Head Neck Surg.142 (2), 138 – 142 (2016).
   PubMed Web of Science ®Google Scholar
• Liu CM , SoldanovaK, NordstromLet al. Medical therapy reduces microbiota diversity and evenness in surgically recalcitrant chronic rhinosinusitis. Int. Forum Allergy Rhinol. 3 (10), 775 – 781 (2013).
   PubMed Web of Science ®Google Scholar
• Merkley MA , BiceTC, GrierA, StrohlAM, ManLX, GillSR. The effect of antibiotics on the microbiome in acute exacerbations of chronic rhinosinusitis.Int. Forum Allergy Rhinol.5 (10), 884 – 893 (2015).
   PubMed Web of Science ®Google Scholar
• Chan BK , AbedonST. Phage therapy pharmacology: phage cocktails.Adv. Appl. Microbiol.78, 1 – 23 (2012).
   PubMed Web of Science ®Google Scholar
• Bruttin A , BrussowH. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy.Antimicrob. Agents Chemother.49 (7), 2874 – 2878 (2005).
   PubMed Web of Science ®Google Scholar
• Sarker SA , MccallinS, BarrettoCet al. Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology 434 (2), 222 – 232 (2012).
   PubMed Web of Science ®Google Scholar
• Singhal D , PsaltisAJ, ForemanA, WormaldPJ. The impact of biofilms on outcomes after endoscopic sinus surgery.Am. J. Rhinol. Allergy24 (3), 169 – 174 (2010).
   PubMed Web of Science ®Google Scholar
• Zhang Z , LinkinDR, FinkelmanBSet al. Asthma and biofilm-forming bacteria are independently associated with revision sinus surgeries for chronic rhinosinusitis. J. Allergy Clin. Immunol. 128 (1), 221 – 223 (2011).
   PubMed Web of Science ®Google Scholar
• Mladina R , SkitarelicN, MusicS, RisticM. A biofilm exists on healthy mucosa of the paranasal sinuses: a prospectively performed, blinded, scanning electron microscope study.Clin. Otolaryngol.35 (2), 104 – 110 (2010).
   PubMed Web of Science ®Google Scholar
• Sanderson AR , LeidJG, HunsakerD. Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis.Laryngoscope116 (7), 1121 – 1126 (2006).
   PubMed Web of Science ®Google Scholar
• Post JC , StoodleyP, Hall-StoodleyL, EhrlichGD. The role of biofilms in otolaryngologic infections.Curr. Opin. Otolaryngol. Head Neck Surg.12 (3), 185 – 190 (2004).
   PubMedGoogle Scholar
• Post JC , HillerNL, NisticoL, StoodleyP, EhrlichGD. The role of biofilms in otolaryngologic infections: update 2007.Curr. Opin. Otolaryngol. Head Neck Surg.15 (5), 347 – 351 (2007).
   PubMedGoogle Scholar
• Foreman A , Jervis-BardyJ, WormaldPJ. Do biofilms contribute to the initiation and recalcitrance of chronic rhinosinusitis?Laryngoscope121 (5), 1085 – 1091 (2011).
   PubMed Web of Science ®Google Scholar
• Cohen M , KofonowJ, NayakJVet al. Biofilms in chronic rhinosinusitis: a review. Am. J. Rhinol. Allergy 23 (3), 255 – 260 (2009).
   PubMed Web of Science ®Google Scholar
• Singh P , MehtaR, AgarwalS, MishraP. Bacterial biofilm on the sinus mucosa of healthy subjects and patients with chronic rhinosinusitis (with or without nasal polyposis).J. Laryngol. Otol.129 (1), 46 – 49 (2015).
   PubMed Web of Science ®Google Scholar
• Foreman A , PsaltisAJ, TanLW, WormaldPJ. Characterization of bacterial and fungal biofilms in chronic rhinosinusitis.Am. J. Rhinol. Allergy23 (6), 556 – 561 (2009).
   PubMed Web of Science ®Google Scholar
• Psaltis AJ , HaMR, BeuleAG, TanLW, WormaldPJ. Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis.Laryngoscope117 (7), 1302 – 1306 (2007).
   PubMed Web of Science ®Google Scholar
• Sanclement JA , WebsterP, ThomasJ, RamadanHH. Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis.Laryngoscope115 (4), 578 – 582 (2005).
   PubMed Web of Science ®Google Scholar
• Galli J , CaloL, ArditoFet al. Damage to ciliated epithelium in chronic rhinosinusitis: what is the role of bacterial biofilms? Ann. Otol. Rhinol. Laryngol. 117 (12), 902 – 908 (2008).
   PubMed Web of Science ®Google Scholar
• Healy DY , LeidJG, SandersonAR, HunsakerDH. Biofilms with fungi in chronic rhinosinusitis.Otolaryngol. Head Neck Surg.138 (5), 641 – 647 (2008).
   PubMed Web of Science ®Google Scholar
• Foreman A , WormaldPJ. Different biofilms, different disease? A clinical outcomes study.Laryngoscope120 (8), 1701 – 1706 (2010).
   PubMed Web of Science ®Google Scholar
• Bendouah Z , BarbeauJ, HamadWA, DesrosiersM. Biofilm formation by Staphylococcus aureus and Pseudomonas aeruginosa is associated with an unfavorable evolution after surgery for chronic sinusitis and nasal polyposis.Otolaryngol. Head Neck Surg.134 (6), 991 – 996 (2006).
   PubMed Web of Science ®Google Scholar
• Singhal D , ForemanA, Jervis-BardyJ, WormaldPJ. Staphylococcus aureus biofilms: nemesis of endoscopic sinus surgery.Laryngoscope121 (7), 1578 – 1583 (2011).
   PubMed Web of Science ®Google Scholar
• Zhang Z , HanDM, ZhangSZet al. Biofilms and mucosal healing in postsurgical patients with chronic rhinosinusitis. Am. J. Rhinol. Allergy 23 (5), 506 – 511 (2009).
   PubMed Web of Science ®Google Scholar
• Kalishwaralal K , BarathmanikanthS, PandianSRK, DeepakV, GurunathanS. Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis.Colloids Surf. B. Biointerfaces79 (2), 340 – 344 (2010).
   PubMed Web of Science ®Google Scholar
• Markowska K , GrudniakAM, WolskaKI. Silver nanoparticles as an alternative strategy against bacterial biofilms.Acta Biochim. Pol.60 (4), 523 – 530 (2013).
   PubMed Web of Science ®Google Scholar
• Ramakrishnan Y , ShieldsRC, ElbadaweyMR, WilsonJA. Biofilms in chronic rhinosinusitis: what is new and where next?J. Laryngol. Otol.129 (8), 744 – 751 (2015).
   PubMed Web of Science ®Google Scholar
• Jain R , DouglasR. When and how should we treat biofilms in chronic sinusitis?Curr. Opin. Otolaryngol. Head Neck Surg.22 (1), 16 – 21 (2014).
   PubMed Web of Science ®Google Scholar
• Briandet R , Lacroix-GueuP, RenaultMet al. Fluorescence correlation spectroscopy to study diffusion and reaction of bacteriophages inside biofilms. Appl. Environ. Microbiol. 74 (7), 2135 – 2143 (2008).
   PubMed Web of Science ®Google Scholar
• Doolittle MM , CooneyJJ, CaldwellDE. Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes.J. Ind. Microbiol.16 (6), 331 – 341 (1996).
   PubMedGoogle Scholar
• Azeredo J , SutherlandIW. The use of phages for the removal of infectious biofilms.Curr. Pharm. Biotechnol.9 (4), 261 – 266 (2008).
   PubMed Web of Science ®Google Scholar
• Sutherland IW , HughesKA, SkillmanLC, TaitK. The interaction of phage and biofilms.FEMS Microbiol. Lett.232 (1), 1 – 6 (2004).
   PubMed Web of Science ®Google Scholar
• Abedon ST . Ecology of anti-biofilm agents II: bacteriophage exploitation and biocontrol of biofilm bacteria.Pharmaceuticals (Basel)8 (3), 559 – 589 (2015).
   PubMedGoogle Scholar
• Tait K , SkillmanLC, SutherlandIW. The efficacy of bacteriophage as a method of biofilm eradication.Biofouling18 (4), 305 – 311 (2002).
   Web of Science ®Google Scholar
• Motlagh AM , BhattacharjeeAS, GoelR. Biofilm control with natural and genetically-modified phages.World J. Microbiol. Biotechnol.32 (4), 67 (2016).
   PubMed Web of Science ®Google Scholar
• Bedi MS , VermaV, ChhibberS. Amoxicillin and specific bacteriophage can be used together for eradication of biofilm of Klebsiella pneumoniae B5055.World J. Microbiol. Biotechnol.25 (7), 1145 – 1151 (2009).
   Web of Science ®Google Scholar
• Ryan EM , AlkawareekMY, DonnellyRF, GilmoreBF. Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro.FEMS Immunol. Med. Microbiol.65 (2), 395 – 398 (2012).
   PubMedGoogle Scholar
• Comeau AM , TetartF, TrojetSN, PrereMF, KrischHM. Phage-antibiotic synergy (PAS): beta-lactam and quinolone antibiotics stimulate virulent phage growth.PLoS ONE2 (8), e799 (2007).
   PubMed Web of Science ®Google Scholar
• Prince AA , SteigerJD, KhalidANet al. Prevalence of biofilm-forming bacteria in chronic rhinosinusitis. Am. J. Rhinol. 22 (3), 239 – 245 (2008).
   PubMedGoogle Scholar
• Burmolle M , WebbJS, RaoD, HansenLH, SorensenSJ, KjellebergS. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms.Appl. Environ. Microbiol.72 (6), 3916 – 3923 (2006).
   PubMed Web of Science ®Google Scholar
• Rickard AH , GilbertP, HighNJ, KolenbranderPE, HandleyPS. Bacterial coaggregation: an integral process in the development of multi-species biofilms.Trends Microbiol.11 (2), 94 – 100 (2003).
   PubMed Web of Science ®Google Scholar
• Skillman LC , SutherlandIW, JonesMV. The role of exopolysaccharides in dual species biofilm development.J. Appl. Microbiol.85, 13s – 18s (1999).
   Web of Science ®Google Scholar
• Gonzalez S , FernandezL, CampeloABet al. The behavior of Staphylococcus aureus dual-species biofilms treated with bacteriophage phiIPLA-RODI depends on the accompanying microorganism. Appl. Environ. Microbiol. 83 (3), pii: e02821–16 (2017).
   Web of Science ®Google Scholar
• Lynch AS , RobertsonGT. Bacterial and fungal biofilm infections.Annu. Rev. Med.59, 415 – 428 (2008).
   PubMed Web of Science ®Google Scholar
• Tan NCW , ForemanA, JardelezaC, DouglasR, TranH, WormaldPJ. The multiplicity of Staphylococcus aureus in chronic rhinosinusitis: correlating surface biofilm and intracellular residence.Laryngoscope122 (8), 1655 – 1660 (2012).
   PubMed Web of Science ®Google Scholar
• Capparelli R , ParlatoM, BorrielloG, SalvatoreP, IannelliD. Experimental phage therapy against Staphylococcus aureus in mice.Antimicrob. Agents Chemother.51 (8), 2765 – 2773 (2007).
   PubMed Web of Science ®Google Scholar
• Zhang LL , SunLC, WeiRCet al. Intracellular Staphylococcus aureus control by virulent bacteriophages within MAC-T bovine mammary epithelial cells. Antimicrob. Agents Chemother. doi:10.1128/AAC.01990-16 (2017 ) ( Epub ahead of print).
   Web of Science ®Google Scholar
• Abedon ST . Bacteriophages as Drugs: the Pharmacology of Phage Therapy. In : Phage Therapy: Current Research and Applications. BorysowskiJ, MiędzybrodzkiR, GórskiA( Eds ). Caister Academic Press, Norfolk, UK, 69 – 100 (2014).
   Google Scholar
• Liang J , LaneAP. Topical drug delivery for chronic rhinosinusitis.Curr. Otorhinolaryngol. Rep.1 (1), 51 – 60 (2013).
   PubMedGoogle Scholar
• Jervis-Bardy J , BoaseS, PsaltisA, ForemanA, WormaldPJ. A randomized trial of mupirocin sinonasal rinses versus saline in surgically recalcitrant staphylococcal chronic rhinosinusitis.Laryngoscope122 (10), 2148 – 2153 (2012).
   PubMed Web of Science ®Google Scholar
• Kim JS , KwonSH. Mupirocin in the treatment of staphylococcal infections in chronic rhinosinusitis: a meta-analysis.PLoS ONE11 (12), e0167369 (2016).
   PubMed Web of Science ®Google Scholar
• Rudmik L , HoyM, SchlosserRJet al. Topical therapies in the management of chronic rhinosinusitis: an evidence-based review with recommendations. Int. Forum Allergy Rhinol. 3 (4), 281 – 298 (2013).
   PubMed Web of Science ®Google Scholar
• Leung SSY , ParumasivamT, GaoFGet al. Effects of storage conditions on the stability of spray dried, inhalable bacteriophage powders. Int. J. Pharm. 521 (1–2), 141 – 149 (2017).
   PubMedGoogle Scholar
• Alfadhel M , PuapermpoonsiriU, FordSJ, McinnesFJ, Van Der WalleCF. Lyophilized inserts for nasal administration harboring bacteriophage selective for Staphylococcus aureus: in vitro evaluation.Int. J. Pharm.416 (1), 280 – 287 (2011).
   PubMed Web of Science ®Google Scholar
• Weber-Dabrowska B , Jonczyk-MatysiakE, ZaczekM, LobockaM, Lusiak-SzelachowskaM, GorskiA. Bacteriophage procurement for therapeutic purposes.Front. Microbiol.7, 1177 (2016).
   PubMed Web of Science ®Google Scholar
• Drilling A , MoralesS, JardelezaC, VreugdeS, SpeckP, WormaldPJ. Bacteriophage reduces biofilm of Staphylococcus aureus ex vivo isolates from chronic rhinosinusitis patients.Am. J. Rhinol. Allergy28 (1), 3 – 11 (2014).
   PubMed Web of Science ®Google Scholar
• Drilling AJ , CooksleyC, ChanC, WormaldPJ, VreugdeS. Fighting sinus-derived Staphylococcus aureus biofilms in vitro with a bacteriophage-derived muralytic enzyme.Int. Forum Allergy Rhinol.6 (4), 349 – 355 (2016).
   PubMed Web of Science ®Google Scholar
• Chhibber S , GuptaP, KaurS. Bacteriophage as effective decolonising agent for elimination of MRSA from anterior nares of BALB/c mice.BMC Microbiol.14, 212 (2014).
   PubMed Web of Science ®Google Scholar
• Fenton M , CaseyPG, HillCet al. The truncated phage lysin CHAP(k) eliminates Staphylococcus aureus in the nares of mice. Bioengineered Bugs 1 (6), 404 – 407 (2010).
   PubMedGoogle Scholar
• Drilling A , MoralesS, BoaseSet al. Safety and efficacy of topical bacteriophage and ethylenediaminetetraacetic acid treatment of Staphylococcus aureus infection in a sheep model of sinusitis. Int. Forum Allergy Rhinol. 4 (3), 176 – 186 (2014).
   PubMed Web of Science ®Google Scholar
• Drilling AJ , OoiML, MiljkovicDet al. Long-term safety of topical bacteriophage application to the frontal sinus region. Front. Cell. Infect. Microbiol. doi:10.3389/fcimb.2017.00049 (2017 ) ( Epub ahead of print).
   Web of Science ®Google Scholar
• Mills AE . Staphylococcus bacteriophage lysate aerosol therapy of sinusitis.Laryngoscope66 (7), 846 – 858 (1956).
   PubMedGoogle Scholar
• Weber-Dabrowska B , KoźmińskaJ, MulczykM, KaczkowskiH. Wykorzystanie bakteriofagów w leczeniu przewlekłego ropnego zapalenia zatok szczękowych.Post. Med. Klin. Dośw.5 (3), 291 – 293 (1996).
   Google Scholar
• Weber-Dabrowska B , MulczykM, GórskiA. Bacteriophage therapy of bacterial infectons: an update on our institute's experience.Arch. Immunol. Ther. Exp. (Warsz.)48 (6), 547 – 551 (2000).
   PubMedGoogle Scholar
• AmpliPhi Biosciences Corporation . www.ampliphibio.com/product-pipeline.
   Google Scholar
• Lebeaux D , ChauhanA, RenduelesO, BeloinC. From in vitro to in vivo models of bacterial biofilm-related infections.Pathogens2 (2), 288 – 356 (2013).
   PubMedGoogle Scholar
• Leon M , BastiasR. Virulence reduction in bacteriophage resistant bacteria.Front. Microbiol.6, 343 (2015).
   PubMed Web of Science ®Google Scholar
• Mann NH . The potential of phages to prevent MRSA infections.Res. Microbiol.159 (5), 400 – 405 (2008).
   PubMed Web of Science ®Google Scholar
• Ha KR , PsaltisAJ, TanL, WormaldPJ. A sheep model for the study of biofilms in rhinosinusitis.Am. J. Rhinol.21 (3), 339 – 345 (2007).
   PubMedGoogle Scholar
• Belum GR , BelumVR, Chaitanya ArudraSK, ReddyBS. The Jarisch–Herxheimer reaction: revisited.Travel Med. Infect. Dis.11 (4), 231 – 237 (2013).
   PubMed Web of Science ®Google Scholar
• Herxheimer K , KrauseN. Ueber eine bei Syphilitischen vorkommende Quecksilberreaktion.Dtsch. Med. Wochenschr.28 (50), 895 – 897 (1902).
   Google Scholar
• Gorski A , DabrowskaK, MiedzybrodzkiRet al. Phages and immunomodulation. Future Microbiol. 12 (10), 905 – 914 (2017).
   PubMed Web of Science ®Google Scholar
• Wright A , HawkinsCH, AnggardEE, HarperDR. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy.Clin. Otolaryngol.34 (4), 349 – 357 (2009).
   PubMed Web of Science ®Google Scholar
• Parsons DS , WaldER. Otitis media and sinusitis: similar diseases.Otolaryngol. Clin. North Am.29 (1), 11 – 25 (1996).
   PubMed Web of Science ®Google Scholar
• Wald ER . Acute otitis media and acute bacterial sinusitis.Clin. Infect. Dis.52 (Suppl. 4), S277 – S283 (2011).
   PubMedGoogle Scholar
• Marchisio P , GhisalbertiE, FusiM, BaggiE, RagazziM, DusiE. Paranasal sinuses and middle ear infections: what do they have in common?Pediatr. Allergy Immunol.18 (Suppl. 18), 31 – 34 (2007).
   PubMedGoogle Scholar
• Coates T , BaxR, CoatesA. Nasal decolonization of Staphylococcus aureus with mupirocin: strengths, weaknesses and future prospects.J. Antimicrob. Chemother.64 (1), 9 – 15 (2009).
   PubMed Web of Science ®Google Scholar
• Fairhead H . SASP gene delivery: a novel antibacterial approach.Drug News Perspect22 (4), 197 – 203 (2009).
   PubMed Web of Science ®Google Scholar
• Nosulya EV . Prospects for the application of bacteriophages in otorhinolaryngology.Vestn. Otorinolaringol.1, 80 – 83 (2015).
   Google Scholar
• Briusov PG , ZubritskiiVF, IslamovRN, NizovoiAV, FominykhEM. Phagoprophylaxis and bacteriophage treatment of surgical infections.Voen. Med. Zh.332 (4), 34 – 39 (2011).
   PubMedGoogle Scholar
• Biomedservice. Otofag. https://b2brazil.com/hotsite/biomedservice/otofag.
   Google Scholar
• Microgen . Sextaphag® polyvalent pyobacteriophage.www.microgen.ru/en/products/bakteriofagi/sekstafag-piobakteriofag-polivalentnyy/.
   Google Scholar
• Phage Therapy Center's Treatment of Rhinosinusitis. www.phagetherapycenter.com/pii/PatientServlet?command=static_sinusitis.
   Google Scholar