Generic placeholder image

Recent Patents on Biotechnology

Editor-in-Chief

ISSN (Print): 1872-2083
ISSN (Online): 2212-4012

Review Article

Review on Stenotrophomonas maltophilia: An Emerging Multidrug- resistant Opportunistic Pathogen

Author(s): Rikhia Majumdar, Hariharan Karthikeyan, Vaishnavi Senthilnathan and Shobana Sugumar*

Volume 16, Issue 4, 2022

Published on: 07 July, 2022

Page: [329 - 354] Pages: 26

DOI: 10.2174/1872208316666220512121205

Price: $65

Abstract

Stenotrophomonas maltophilia is an opportunistic pathogen that results in nosocomial infections in immunocompromised individuals. These bacteria colonize on the surface of medical devices and therapeutic equipment like urinary catheters, endoscopes, and ventilators, causing respiratory and urinary tract infections. The low outer membrane permeability of multidrug-resistance efflux systems and the two chromosomally encoded β- lactamases present in S. maltophilia are challenging for arsenal control. The cell-associated and extracellular virulence factors in S. maltophilia are involved in colonization and biofilm formation on the host surfaces. The spread of antibiotic-resistant genes in the pathogenic S. maltophilia attributes to bacterial resistance against a wide range of antibiotics, including penicillin, quinolones, and carbapenems. So far, tetracycline derivatives, fluoroquinolones, and trimethoprim-sulfamethoxazole (TMP-SMX) are considered promising antibiotics against S. maltophilia. Due to the adaptive nature of the intrinsically resistant mechanism towards the number of antibiotics and its ability to acquire new resistance via mutation and horizontal gene transfer, it is quite tricky for medicinal contribution against S. maltophilia. The current review summarizes the literary data on pathogenicity, quorum sensing, biofilm formation, virulence factors, and antibiotic resistance of S. maltophilia.

Keywords: Antibiotic resistance, biofilm, virulence factors, Stenotrophomonas maltophilia, antimicrobial, β-lactams.

Graphical Abstract

[1]
Gnanasekaran I, Bajaj R. Stenotrophomonas maltophilia bacteremia in end-stage renal disease patients receiving maintenance hemodialysis. Dial Transplant 2009; 38(1): 30-2.
[http://dx.doi.org/10.1002/dat.20276]
[2]
Muder RR, Yu VL, Dummer JS, Vinson C, Lumish RM. Infections caused by Pseudomonas maltophilia. Expanding clinical spectrum. Arch Intern Med 1987; 147(9): 1672-4.
[http://dx.doi.org/10.1001/archinte.1987.00370090148025] [PMID: 3632174]
[3]
Calza L, Manfredi R, Chiodo F. Stenotrophomonas (Xanthomonas) maltophilia as an emerging opportunistic pathogen in association with HIV infection: A 10-year surveillance study. Infection 2003; 31(3): 155-61.
[http://dx.doi.org/10.1007/s15010-003-3113-6] [PMID: 12789473]
[4]
Cernohorská L, Votava M. Determination of Minimal Regrowth Concentration (MRC) in clinical isolates of various biofilm-forming bacteria. Folia Microbiol 2004; 49(1): 75-8.
[http://dx.doi.org/10.1007/BF02931650] [PMID: 15114870]
[5]
Yeshurun M, Gafter-Gvili A, Thaler M, Keller N, Nagler A, Shimoni A. Clinical characteristics of Stenotrophomonas maltophilia infection in hematopoietic stem cell transplantation recipients: A single center experience. Infection 2010; 38(3): 211-5.
[http://dx.doi.org/10.1007/s15010-010-0023-2] [PMID: 20425134]
[6]
Hentrich M, Schalk E, Schmidt-Hieber M, et al. Central venous catheter-related infections in hematology and oncology: 2012 updated guidelines on diagnosis, management and prevention by the Infectious Diseases Working Party of the German Society of Hematology and Medical Oncology. Ann Oncol 2014; 25(5): 936-47.
[http://dx.doi.org/10.1093/annonc/mdt545] [PMID: 24399078]
[7]
Adegoke AA, Stenström TA, Okoh AI. Stenotrophomonas maltophilia as an emerging ubiquitous pathogen: Looking beyond contemporary antibiotic therapy. Front Microbiol 2017; 8: 2276.
[http://dx.doi.org/10.3389/fmicb.2017.02276] [PMID: 29250041]
[8]
Börner D, Marsch WC, Fischer M. Necrotizing otitis externa caused by Stenotrophomonas maltophilia. Hautarzt 2003; 54(11): 1080-2.
[http://dx.doi.org/10.1007/s00105-003-0551-0]
[9]
Berg G, Rybakova D, Grube M, Köberl M. The plant microbiome explored: Implications for experimental botany. J Exp Bot 2016; 67(4): 995-1002.
[http://dx.doi.org/10.1093/jxb/erv466] [PMID: 26547794]
[10]
Furushita M, Okamoto A, Maeda T, Ohta M, Shiba T. Isolation of multidrug-resistant Stenotrophomonas maltophilia from cultured yellowtail (Seriola quinqueradiata) from a marine fish farm. Appl Environ Microbiol 2005; 71(9): 5598-600.
[http://dx.doi.org/10.1128/AEM.71.9.5598-5600.2005] [PMID: 16151156]
[11]
Gilligan PH, Lum G, Vandamme P, Whittier S. Burkholderia, Stenotrophomonas, Ralstonia, Brevundimonas, Comamonas, Delftia, Pandoraea and Acidovorax Manual of Clinical Microbiology 2003; 729-48.
[12]
Brooke JS. Stenotrophomonas maltophilia: An emerging global opportunistic pathogen. Clin Microbiol Rev 2012; 25(1): 2-41.
[http://dx.doi.org/10.1128/CMR.00019-11] [PMID: 22232370]
[13]
Nseir S, Di Pompeo C, Brisson H, et al. Intensive care unit-acquired Stenotrophomonas maltophilia: Incidence, risk factors, and outcome. Crit Care 2006; 10(5): R143.
[http://dx.doi.org/10.1186/cc5063] [PMID: 17026755]
[14]
Demiraslan H, Sevim M, Pala Ç, et al. Risk factors influencing mortality related to Stenotrophomonas maltophilia infection in hematology-oncology patients. Int J Hematol 2013; 97(3): 414-20.
[http://dx.doi.org/10.1007/s12185-013-1296-x] [PMID: 23430671]
[15]
Waters V, Atenafu EG, Lu A, Yau Y, Tullis E, Ratjen F. Chronic Stenotrophomonas maltophilia infection and mortality or lung transplantation in cystic fibrosis patients. J Cyst Fibros 2013; 12(5): 482-6.
[http://dx.doi.org/10.1016/j.jcf.2012.12.006] [PMID: 23294530]
[16]
Scholte JB, Zhou TL, Bergmans DC, et al. Stenotrophomonas maltophilia ventilator-associated pneumonia. A retrospective matched case-control study. Infect Dis 2016; 48(10): 738-43.
[http://dx.doi.org/10.1080/23744235.2016.1185534] [PMID: 27207483]
[17]
Denton M, Kerr KG. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 1998; 11(1): 57-80.
[http://dx.doi.org/10.1128/CMR.11.1.57] [PMID: 9457429]
[18]
Meyer E, Schwab F, Gastmeier P, Rueden H, Daschner FD, Jonas D. Stenotrophomonas maltophilia and antibiotic use in German intensive care units: Data from Project SARI (Surveillance of Antimicrobial Use and Antimicrobial Resistance in German Intensive Care Units). J Hosp Infect 2006; 64(3): 238-43.
[http://dx.doi.org/10.1016/j.jhin.2006.07.006] [PMID: 16979794]
[19]
Sánchez MB. Antibiotic resistance in the opportunistic pathogen Stenotrophomonas maltophilia. Front Microbiol 2015; 6: 658.
[http://dx.doi.org/10.3389/fmicb.2015.00658] [PMID: 26175724]
[20]
Hamdi AM, Fida M, Abu Saleh OM, Beam E. Stenotrophomonas bacteremia antibiotic susceptibility and prognostic determinants: Mayo clinic 10-year experience. Open Forum Infect Dis 2020; 7(1): a008.
[http://dx.doi.org/10.1093/ofid/ofaa008] [PMID: 32016126]
[21]
Ramirez MS, Tolmasky ME. Drug resistance updates: Reviews and commentaries in antimicrobial and anticancer chemotherapy. Aminoglyc Mod Enzymes 2010; 13(6): 151-71.
[http://dx.doi.org/10.1016/j.drup.2010.08.003]
[22]
Valdezate S, Vindel A, Echeita A, Baquero F, Cantó R. Topoisomerase II and IV quinolone resistance-determining regions in Stenotrophomonas maltophilia clinical isolates with different levels of quinolone susceptibility. Antimicrob Agents Chemother 2002; 46(3): 665-71.
[http://dx.doi.org/10.1128/AAC.46.3.665-671.2002] [PMID: 11850246]
[23]
van Duijkeren E, Schink AK, Roberts MC, Wang Y, Schwarz S. Mechanisms of bacterial resistance to antimicrobial agents Microbiol Spectr 2018; 6(1 2): 6-12.
[http://dx.doi.org/10.1128/microbiolspec.ARBA-0019-2017] [PMID: 29327680]
[24]
Falagas ME, Kastoris AC, Vouloumanou EK, Rafailidis PI, Kapaskelis AM, Dimopoulos G. Attributable mortality of Stenotrophomonas maltophilia infections: A systematic review of the literature. Future Microbiol 2009; 4(9): 1103-9.
[http://dx.doi.org/10.2217/fmb.09.84] [PMID: 19895214]
[25]
Zemanick ET, Wagner BD, Robertson CE, et al. Airway microbiota across age and disease spectrum in cystic fibrosis. Eur Respir J 2017; 50(5)1700832
[http://dx.doi.org/10.1183/13993003.00832-2017] [PMID: 29146601]
[26]
Pek Z, Cabanilla MG, Ahmed S. Treatment refractory Stenotrophomonas maltophilia bacteraemia and pneumonia in a COVID-19-positive patient. BMJ Case Reports CP 2021; 14e242670
[27]
Huang YW, Hu RM, Chu FY, Lin HR, Yang TC. Characterization of a Major Facilitator Superfamily (MFS) tripartite efflux pump EmrCABsm from Stenotrophomonas maltophilia. J Antimicrob Chemother 2013; 68(11): 2498-505.
[http://dx.doi.org/10.1093/jac/dkt250] [PMID: 23794602]
[28]
Jones RN. Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clin Infect Dis 2010; 51(Suppl. 1): S81-7.
[http://dx.doi.org/10.1086/653053] [PMID: 20597676]
[29]
Kim JH, Kim SW, Kang HR, et al. Two episodes of Stenotrophomonas maltophilia endocarditis of prosthetic mitral valve: Report of a case and review of the literature. J Korean Med Sci 2002; 17(2): 263-5.
[http://dx.doi.org/10.3346/jkms.2002.17.2.263] [PMID: 11961315]
[30]
Bottone EJ, Reitano M, Janda JM, Troy K, Cuttner J. Pseudomonas maltophilia exoenzyme activity as correlate in pathogenesis of ecthyma gangrenosum. J Clin Microbiol 1986; 24(6): 995-7.
[http://dx.doi.org/10.1128/jcm.24.6.995-997.1986] [PMID: 3537006]
[31]
Di Bonaventura G, Stepanović S, Picciani C, Pompilio A, Piccolomini R. Effect of environmental factors on biofilm formation by clinical Stenotrophomonas maltophilia isolates. Folia Microbiol 2007; 52(1): 86-90.
[http://dx.doi.org/10.1007/BF02932144] [PMID: 17571802]
[32]
Fouhy Y, Scanlon K, Schouest K, et al. Diffusible signal factor-dependent cell-cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia. J Bacteriol 2007; 189(13): 4964-8.
[http://dx.doi.org/10.1128/JB.00310-07] [PMID: 17468254]
[33]
Thomas J, Prabhu VN, Varaprasad IR, Agrawal S, Narsimulu G. Stenotrophomonas maltophilia: A very rare cause of tropical pyomyositis. Int J Rheum Dis 2010; 13(1): 89-90.
[http://dx.doi.org/10.1111/j.1756-185X.2009.01447.x] [PMID: 20374391]
[34]
Weber DJ, Rutala WA, Sickbert-Bennett EE, Samsa GP, Brown V, Niederman MS. Microbiology of ventilator-associated pneumonia compared with that of hospital-acquired pneumonia. Infect Control Hosp Epidemiol 2007; 28(7): 825-31.
[http://dx.doi.org/10.1086/518460] [PMID: 17564985]
[35]
Pathmanathan A, Waterer GW. Significance of positive Stenotrophomonas maltophilia culture in acute respiratory tract infection. Eur Respir J 2005; 25(5): 911-4.
[http://dx.doi.org/10.1183/09031936.05.00096704] [PMID: 15863651]
[36]
Senol E. Stenotrophomonas maltophilia: The significance and role as a nosocomial pathogen. J Hosp Infect 2004; 57(1): 1-7.
[http://dx.doi.org/10.1016/j.jhin.2004.01.033] [PMID: 15142709]
[37]
Lai CH, Chi CY, Chen HP, et al. Clinical characteristics and prognostic factors of patients with Stenotrophomonas maltophilia bacteremia. J Microbiol Immunol Infect 2004; 37(6): 350-8.
[PMID: 15599467]
[38]
Rolston KV, Kontoyiannis DP, Yadegarynia D, Raad II. Nonfermentative gram-negative bacilli in cancer patients: Increasing frequency of infection and antimicrobial susceptibility of clinical isolates to fluoroquinolones. Diagn Microbiol Infect Dis 2005; 51(3): 215-8.
[http://dx.doi.org/10.1016/j.diagmicrobio.2004.11.002] [PMID: 15766609]
[39]
Krzewinski JW, Nguyen CD, Foster JM, Burns JL. Use of random amplified polymorphic DNA PCR to examine epidemiology of Stenotrophomonas maltophilia and Achromobacter (Alcaligenes) xylosoxidans from patients with cystic fibrosis. J Clin Microbiol 2001; 39(10): 3597-602.
[http://dx.doi.org/10.1128/JCM.39.10.3597-3602.2001] [PMID: 11574579]
[40]
Huang TP, Somers EB, Wong AC. Differential biofilm formation and motility associated with lipopolysaccharide/exopolysaccharide-coupled biosynthetic genes in Stenotrophomonas maltophilia. J Bacteriol 2006; 188(8): 3116-20.
[http://dx.doi.org/10.1128/JB.188.8.3116-3120.2006] [PMID: 16585771]
[41]
LaSarre B, Federle MJ. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 2013; 77(1): 73-111.
[http://dx.doi.org/10.1128/MMBR.00046-12] [PMID: 23471618]
[42]
Krause KM, Serio AW, Kane TR, Connolly LE. Aminoglycosides: An overview. Cold Spring Harb Perspect Med 2016; 6(6)a027029
[http://dx.doi.org/10.1101/cshperspect.a027029] [PMID: 27252397]
[43]
García CA, Alcaraz ES, Franco MA, Passerini de Rossi BN. Iron is a signal for Stenotrophomonas maltophilia biofilm formation, oxidative stress response, OMPs expression, and virulence. Front Microbiol 2015; 6: 926.
[http://dx.doi.org/10.3389/fmicb.2015.00926] [PMID: 26388863]
[44]
Alonso A, Martínez JL. Multiple antibiotic resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 1997; 41(5): 1140-2.
[http://dx.doi.org/10.1128/AAC.41.5.1140] [PMID: 9145884]
[45]
Suppiger A, Eshwar AK, Stephan R, Kaever V, Eberl L, Lehner A. The DSF type quorum sensing signalling system RpfF/R regulates diverse phenotypes in the opportunistic pathogen Cronobacter. Sci Rep 2016; 6: 18753.
[http://dx.doi.org/10.1038/srep18753] [PMID: 26725701]
[46]
Duan Z, Qin J, Li C, Ying C. Clinical and molecular epidemiology of Stenotrophomonas maltophilia in pediatric patients from a Chinese teaching hospital. Front Cell Infect Microbiol 2020; 10: 411.
[http://dx.doi.org/10.3389/fcimb.2020.00411] [PMID: 32850503]
[47]
Cruz-Córdova A, Mancilla-Rojano J, Luna-Pineda VM, et al. Molecular epidemiology, antibiotic resistance, and virulence traits of Stenotrophomonas maltophilia strains associated with an outbreak in a Mexican tertiary care hospital. Front Cell Infect Microbiol 2020; 10: 50.
[http://dx.doi.org/10.3389/fcimb.2020.00050] [PMID: 32133303]
[48]
Capaldo C, Beauruelle C, Saliou P, Rault G, Ramel S, Héry-Arnaud G. Investigation of Stenotrophomonas maltophilia epidemiology in a French cystic fibrosis center. Respir Med Res 2020; 78100757
[http://dx.doi.org/10.1016/j.resmer.2020.100757] [PMID: 32759054]
[49]
Waters VJ, Gómez MI, Soong G, Amin S, Ernst RK, Prince A. Immunostimulatory properties of the emerging pathogen Stenotrophomonas maltophilia. Infect Immun 2007; 75(4): 1698-703.
[http://dx.doi.org/10.1128/IAI.01469-06] [PMID: 17220304]
[50]
McKay GA, Woods DE, MacDonald KL, Poole K. Role of phosphoglucomutase of Stenotrophomonas maltophilia in lipopolysaccharide biosynthesis, virulence, and antibiotic resistance. Infect Immun 2003; 71(6): 3068-75.
[http://dx.doi.org/10.1128/IAI.71.6.3068-3075.2003] [PMID: 12761084]
[51]
Vickers IE, Smikle MF. The immunomodulatory effect of antibiotics on the secretion of tumour necrosis factor alpha by peripheral blood mononuclear cells in response to Stenotrophomonas maltophilia stimulation. West Indian Med J 2006; 55(3): 138-41.
[http://dx.doi.org/10.1590/S0043-31442006000300002] [PMID: 17087095]
[52]
Windhorst S, Frank E, Georgieva DN, et al. The major extracellular protease of the nosocomial pathogen Stenotrophomonas maltophilia: Characterization of the protein and molecular cloning of the gene. J Biol Chem 2002; 277(13): 11042-9.
[http://dx.doi.org/10.1074/jbc.M109525200] [PMID: 11796713]
[53]
Kang XM, Wang FF, Zhang H, Zhang Q, Qiana W. Genome-wide identification of genes necessary for biofilm formation by nosocomial pathogen Stenotrophomonas maltophilia reveals that orphan response regulator FsnR is a critical modulator. Appl Environ Microbiol 2015; 81(4): 1200-9.
[http://dx.doi.org/10.1128/AEM.03408-14] [PMID: 25480754]
[54]
Liu W, Tian XQ, Wei JW, et al. BsmR degrades c-di-GMP to modulate biofilm formation of nosocomial pathogen Stenotrophomonas maltophilia. Sci Rep 2017; 7(1): 4665.
[http://dx.doi.org/10.1038/s41598-017-04763-w] [PMID: 28680041]
[55]
Potera C. Forging a link between biofilms and disease. Science 1999; 283(5409): 1837-9.
[http://dx.doi.org/10.1126/science.283.5409.1837]
[56]
Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol 1995; 49: 711-45.
[http://dx.doi.org/10.1146/annurev.mi.49.100195.003431] [PMID: 8561477]
[57]
Pompilio A, Crocetta V, Confalone P, et al. Adhesion to and biofilm formation on IB3-1 bronchial cells by Stenotrophomonas maltophilia isolates from cystic fibrosis patients. BMC Microbiol 2010; 10: 102.
[http://dx.doi.org/10.1186/1471-2180-10-102] [PMID: 20374629]
[58]
Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: A common cause of persistent infections. Science 1999; 284(5418): 1318-22.
[http://dx.doi.org/10.1126/science.284.5418.1318] [PMID: 10334980]
[59]
Nicoletti M, Iacobino A, Prosseda G, et al. Stenotrophomonas maltophilia strains from cystic fibrosis patients: Genomic variability and molecular characterization of some virulence determinants. Int J Med Microbiol 2011; 301(1): 34-43.
[http://dx.doi.org/10.1016/j.ijmm.2010.07.003] [PMID: 20952251]
[60]
Zhuo C, Zhao QY, Xiao SN. The impact of spgM, rpfF, rmlA gene distribution on biofilm formation in Stenotrophomonas maltophilia. PLoS One 2014; 9(10)e108409
[http://dx.doi.org/10.1371/journal.pone.0108409] [PMID: 25285537]
[61]
An SQ, Tang JL. Diffusible signal factor signaling regulates multiple functions in the opportunistic pathogen Stenotrophomonas maltophilia. BMC Res Notes 2018; 11(1): 569.
[http://dx.doi.org/10.1186/s13104-018-3690-1] [PMID: 30097057]
[62]
Huedo P, Yero D, Martínez-Servat S, et al. Two different RPF clusters distributed among a population of Stenotrophomonas maltophilia clinical strains display differential diffusible signal factor production and virulence regulation. J Bacteriol 2014; 196(13): 2431-42.
[http://dx.doi.org/10.1128/JB.01540-14] [PMID: 24769700]
[63]
Huedo P, Yero D, Martinez-Servat S, et al. Decoding the genetic and functional diversity of the DSF quorum-sensing system in Stenotrophomonas maltophilia. Front Microbiol 2015; 6: 761.
[http://dx.doi.org/10.3389/fmicb.2015.00761] [PMID: 26284046]
[64]
AboZahra R. Quorum sensing and interspecies interactions in Stenotrophomonas maltophilia. Microbiol Res J Int 2013; 414-22.
[65]
Vert M, Doi Y, Hellwich KH, et al. Terminology for biorelated polymers and applications (IUPAC Recommendations 2012). Pure Appl Chem 2012; 84(2)
[http://dx.doi.org/10.1351/PAC-REC-10-12-04]
[66]
Limoli DH, Jones CJ, Wozniak DJ. Bacterial extracellular polysaccharides in biofilm formation and function. Microbiol Spectr 2015; 3(3)
[http://dx.doi.org/10.1128/microbiolspec.MB-0011-2014] [PMID: 26185074]
[67]
Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol 2004; 2(2): 95-108.
[http://dx.doi.org/10.1038/nrmicro821] [PMID: 15040259]
[68]
Vega LM, Alvarez PJ, McLean RJC. Bacterial signaling ecology and potential applications during aquatic biofilm construction. Microb Ecol 2014; 68(1): 24-34.
[http://dx.doi.org/10.1007/s00248-013-0321-1] [PMID: 24276538]
[69]
Akova M, Bonfiglio G, Livermore DM. Susceptibility to beta-lactam antibiotics of mutant strains of Xanthomonas maltophilia with high- and low-level constitutive expression of L1 and L2 beta-lactamases. J Med Microbiol 1991; 35(4): 208-13.
[http://dx.doi.org/10.1099/00222615-35-4-208] [PMID: 1941990]
[70]
Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol 2010; 8(9): 623-33.
[http://dx.doi.org/10.1038/nrmicro2415] [PMID: 20676145]
[71]
Mercuri PS, Ishii Y, Ma L, et al. Clonal diversity and metallo-beta-lactamase production in clinical isolates of Stenotrophomonas maltophilia. Microb Drug Resist 2002; 8(3): 193-200.
[http://dx.doi.org/10.1089/107662902760326904] [PMID: 12363008]
[72]
Singh S, Singh SK, Chowdhury I, Singh R. Understanding the mechanism of bacterial biofilms resistance to antimicrobial agents. Open Microbiol J 2017; 11: 53-62.
[http://dx.doi.org/10.2174/1874285801711010053] [PMID: 28553416]
[73]
Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence 2018; 9(1): 522-54.
[http://dx.doi.org/10.1080/21505594.2017.1313372] [PMID: 28362216]
[74]
Hall CW, Mah TF. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev 2017; 41(3): 276-301.
[http://dx.doi.org/10.1093/femsre/fux010] [PMID: 28369412]
[75]
Sharma D, Misba L, Khan AU. Antibiotics versus biofilm: An emerging battleground in microbial communities. Antimicrob Resist Infect Control 2019; 8: 76.
[http://dx.doi.org/10.1186/s13756-019-0533-3] [PMID: 31131107]
[76]
Bostanghadiri N, Ardebili A, Ghalavand Z, et al. Antibiotic resistance, biofilm formation, and biofilm-associated genes among Stenotrophomonas maltophilia clinical isolates. BMC Res Notes 2021; 14(1): 151.
[http://dx.doi.org/10.1186/s13104-021-05567-y] [PMID: 33879237]
[77]
Carattoli A. Plasmid-mediated antimicrobial resistance in Salmonella enterica. Curr Issues Mol Biol 2003; 5(4): 113-22.
[PMID: 12921226]
[78]
Collis CM, Kim MJ, Stokes HW, Hall RM. Binding of the purified integron DNA integrase Intl1 to integron- and cassette-associated recombination sites. Mol Microbiol 1998; 29(2): 477-90.
[http://dx.doi.org/10.1046/j.1365-2958.1998.00936.x] [PMID: 9720866]
[79]
Stokes HW, Tomaras C, Parsons Y, Hall RM. The partial 3′-conserved segment duplications in the integrons In6 from pSa and In7 from pDGO100 have a common origin. Plasmid 1993; 30(1): 39-50.
[http://dx.doi.org/10.1006/plas.1993.1032] [PMID: 8378445]
[80]
Hernández A, Maté MJ, Sánchez-Díaz PC, Romero A, Rojo F, Martínez JL. Structural and functional analysis of SmeT, the repressor of the Stenotrophomonas maltophilia multidrug efflux pump SmeDEF. J Biol Chem 2009; 284(21): 14428-38.
[http://dx.doi.org/10.1074/jbc.M809221200] [PMID: 19324881]
[81]
Falagas ME, Valkimadi PE, Huang YT, Matthaiou DK, Hsueh PR. Therapeutic options for Stenotrophomonas maltophilia infections beyond co-trimoxazole: A systematic review. J Antimicrob Chemother 2008; 62(5): 889-94.
[http://dx.doi.org/10.1093/jac/dkn301] [PMID: 18662945]
[82]
Bostanghadiri N, Ghalavand Z, Fallah F, et al. Characterization of Phenotypic and Genotypic Diversity of Stenotrophomonas maltophilia Strains Isolated From Selected Hospitals in Iran. Front Microbiol 2019; 10: 1191.
[http://dx.doi.org/10.3389/fmicb.2019.01191] [PMID: 31191502]
[83]
Gajdács M, Urbán E. Prevalence and antibiotic resistance of Stenotrophomonas maltophilia in respiratory tract samples: A 10-year epidemiological snapshot. Health Serv Res Manag Epidemiol 2019; 6.
[http://dx.doi.org/10.1177/2333392819870774] [PMID: 31453265]
[84]
Barbolla R, Catalano M, Orman BE, et al. Class 1 integrons increase trimethoprim-sulfamethoxazole MICs against epidemiologically unrelated Stenotrophomonas maltophilia isolates. Antimicrob Agents Chemother 2004; 48(2): 666-9.
[http://dx.doi.org/10.1128/AAC.48.2.666-669.2004] [PMID: 14742234]
[85]
Chang LL, Lin HH, Chang CY, Lu PL. Increased incidence of class 1 integrons in trimethoprim/sulfamethoxazole-resistant clinical isolates of Stenotrophomonas maltophilia. J Antimicrob Chemother 2007; 59(5): 1038-9.
[http://dx.doi.org/10.1093/jac/dkm034] [PMID: 17329265]
[86]
Neela V, Rankouhi SZR, van Belkum A, Goering RV, Awang R. Stenotrophomonas maltophilia in Malaysia: Molecular epidemiology and trimethoprim-sulfamethoxazole resistance. Int J Infect Dis 2012; 16(8): e603-7.
[http://dx.doi.org/10.1016/j.ijid.2012.04.004] [PMID: 22698885]
[87]
Li XZ, Zhang L, McKay GA, Poole K. Role of the acetyltransferase AAC(6′)-Iz modifying enzyme in aminoglycoside resistance in Stenotrophomonas maltophilia. J Antimicrob Chemother 2003; 51(4): 803-11.
[http://dx.doi.org/10.1093/jac/dkg148] [PMID: 12654758]
[88]
Tomich M, Planet PJ, Figurski DH. The tad locus: Postcards from the widespread colonization island. Nat Rev Microbiol 2007; 5(5): 363-75.
[http://dx.doi.org/10.1038/nrmicro1636] [PMID: 17435791]
[89]
Sánchez MB, Martínez JL. The efflux pump SmeDEF contributes to trimethoprim-sulfamethoxazole resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2015; 59(7): 4347-8.
[http://dx.doi.org/10.1128/AAC.00714-15] [PMID: 25918144]
[90]
Hu LF, Chang X, Ye Y, et al. Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 2011; 37(3): 230-4.
[http://dx.doi.org/10.1016/j.ijantimicag.2010.10.025] [PMID: 21296557]
[91]
Lambert T, Ploy MC, Denis F, Courvalin P. Characterization of the chromosomal aac(6′)-Iz gene of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 1999; 43(10): 2366-71.
[http://dx.doi.org/10.1128/AAC.43.10.2366] [PMID: 10508008]
[92]
Okazaki A, Avison MB. Aph(3′)-IIc, an aminoglycoside resistance determinant from Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2007; 51(1): 359-60.
[http://dx.doi.org/10.1128/AAC.00795-06] [PMID: 17088477]
[93]
Tada T, Miyoshi-Akiyama T, Dahal RK, et al. Identification of a novel 6′-N-aminoglycoside acetyltransferase, AAC(6′)-Iak, from a multidrug-resistant clinical isolate of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2014; 58(10): 6324-7.
[http://dx.doi.org/10.1128/AAC.03354-14] [PMID: 25092711]
[94]
Liu MC, Tsai YL, Huang YW, et al. Stenotrophomonas maltophilia PhoP, a two-component response regulator, involved in antimicrobial susceptibilities. PLoS One 2016; 11(5)e0153753
[http://dx.doi.org/10.1371/journal.pone.0153753] [PMID: 27159404]
[95]
Calvopiña K, Dulyayangkul P, Avison MB. Mutations in ribosomal protein RplA or treatment with ribosomal acting antibiotics activates production of aminoglycoside efflux pump SmeYZ in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2020; 64(2): e01524-19.
[http://dx.doi.org/10.1128/AAC.01524-19] [PMID: 31712205]
[96]
Sanchez MB, Hernandez A, Martinez JL. Stenotrophomonas maltophilia drug resistance. Future Microbiol 2009; 4(6): 655-60.
[http://dx.doi.org/10.2217/fmb.09.45] [PMID: 19659422]
[97]
Huang HH, Lin YT, Chen PY, et al. ClpA and HtpX proteases are involved in intrinsic aminoglycoside resistance of Stenotrophomonas maltophilia and are potential aminoglycoside adjuvant targets. Antimicrob Agents Chemother 2018; 62(8): e00554-18.
[http://dx.doi.org/10.1128/AAC.00554-18] [PMID: 29760139]
[98]
Rahmati-Bahram A, Magee JT, Jackson SK. Growth temperature-dependent variation of cell envelope lipids and antibiotic susceptibility in Stenotrophomonas (Xanthomonas) maltophilia. J Antimicrob Chemother 1995; 36(2): 317-26.
[http://dx.doi.org/10.1093/jac/36.2.317] [PMID: 8522461]
[99]
Rahmati-Bahram A, Magee JT, Jackson SK. Temperature-dependent aminoglycoside resistance in Stenotrophomonas (Xanthomonas) maltophilia; alterations in protein and lipopolysaccharide with growth temperature. J Antimicrob Chemother 1996; 37(4): 665-76.
[http://dx.doi.org/10.1093/jac/37.4.665] [PMID: 8722532]
[100]
Chang LL, Chen HF, Chang CY, Lee TM, Wu WJ. Contribution of integrons, and SmeABC and SmeDEF efflux pumps to multidrug resistance in clinical isolates of Stenotrophomonas maltophilia. J Antimicrob Chemother 2004; 53(3): 518-21.
[http://dx.doi.org/10.1093/jac/dkh094] [PMID: 14749340]
[101]
Okazaki A, Avison MB. Induction of L1 and L2 beta-lactamase production in Stenotrophomonas maltophilia is dependent on an AmpR-type regulator. Antimicrob Agents Chemother 2008; 52(4): 1525-8.
[http://dx.doi.org/10.1128/AAC.01485-07] [PMID: 18212097]
[102]
Liaw SJ, Lee YL, Hsueh PR. Multidrug resistance in clinical isolates of Stenotrophomonas maltophilia: Roles of integrons, efflux pumps, phosphoglucomutase (SpgM), and melanin and biofilm formation. Int J Antimicrob Agents 2010; 35(2): 126-30.
[http://dx.doi.org/10.1016/j.ijantimicag.2009.09.015] [PMID: 19926255]
[103]
Lindberg F, Westman L, Normark S. Regulatory components in Citrobacter freundii ampC β-lactamase induction. Proc Natl Acad Sci 1985; 82(14): 4620-4.
[http://dx.doi.org/10.1073/pnas.82.14.4620] [PMID: 2991883]
[104]
Huang YW, Lin CW, Hu RM, Lin YT, Chung TC, Yang TC. AmpN-AmpG operon is essential for expression of L1 and L2 beta-lactamases in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2010; 54(6): 2583-9.
[http://dx.doi.org/10.1128/AAC.01283-09] [PMID: 20385866]
[105]
Liao CH, Chen WC, Li LH, Lin YT, Pan SY, Yang TC. AmpR of Stenotrophomonas maltophilia is involved in stenobactin synthesis and enhanced β-lactam resistance in an iron-depleted condition. J Antimicrob Chemother 2020; 75(12): 3544-51.
[http://dx.doi.org/10.1093/jac/dkaa358] [PMID: 32862228]
[106]
Huang YW, Huang HH, Huang KH, et al. AmpI functions as an iron exporter to alleviate β-Lactam-mediated reactive oxygen species stress in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2019; 63(4): e02467-18.
[http://dx.doi.org/10.1128/AAC.02467-18] [PMID: 30745379]
[107]
Martínez JL, Alonso A, Gómez-Gómez JM, Baquero F. Quinolone resistance by mutations in chromosomal gyrase genes. Just the tip of the iceberg? J Antimicrob Chemother 1998; 42(6): 683-8.
[http://dx.doi.org/10.1093/jac/42.6.683] [PMID: 10052889]
[108]
Trigo Daporta M, Muñoz Bellido JL, García-Rodríguez JA. Topoisomerases mutations and fluoroquinolone resistance in Stenotrophomonas maltophilia. Int J Antimicrob Agents 2004; 24(5): 520-1.
[http://dx.doi.org/10.1016/j.ijantimicag.2004.07.004] [PMID: 15519490]
[109]
Sánchez MB, Martínez JL. SmQnr contributes to intrinsic resistance to quinolones in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2010; 54(1): 580-1.
[http://dx.doi.org/10.1128/AAC.00496-09] [PMID: 19841154]
[110]
Wang M, Sahm DF, Jacoby GA, Hooper DC. Emerging plasmid-mediated quinolone resistance associated with the QNR gene in Klebsiella pneumoniae clinical isolates in the United States. Antimicrob Agents Chemother 2004; 48(4): 1295-9.
[http://dx.doi.org/10.1128/AAC.48.4.1295-1299.2004] [PMID: 15047532]
[111]
Azimi A, Rezaei F, Yaseri M, Jafari S, Rahbar M, Douraghi M. Emergence of fluoroquinolone resistance and possible mechanisms in clinical isolates of Stenotrophomonas maltophilia from Iran. Sci Rep 2021; 11(1): 9582.
[http://dx.doi.org/10.1038/s41598-021-88977-z] [PMID: 33953262]
[112]
Vattanaviboon P, Dulyayangkul P, Mongkolsuk S, Charoenlap N. Overexpression of Stenotrophomonas maltophilia major facilitator superfamily protein MfsA increases resistance to fluoroquinolone antibiotics. J Antimicrob Chemother 2018; 73(5): 1263-6.
[http://dx.doi.org/10.1093/jac/dky024] [PMID: 29462315]
[113]
Du D, Wang-Kan X, Neuberger A, et al. Multidrug efflux pumps: Structure, function and regulation. Nat Rev Microbiol 2018; 16(9): 523-39.
[http://dx.doi.org/10.1038/s41579-018-0048-6] [PMID: 30002505]
[114]
Travassos LH, Pinheiro MN, Coelho FS, Sampaio JL, Merquior VL, Marques EA. Phenotypic properties, drug susceptibility and genetic relatedness of Stenotrophomonas maltophilia clinical strains from seven hospitals in Rio de Janeiro, Brazil. J Appl Microbiol 2004; 96(5): 1143-50.
[http://dx.doi.org/10.1111/j.1365-2672.2004.02248.x] [PMID: 15078532]
[115]
Al-Hamad A, Upton M, Burnie J. Molecular cloning and characterization of SmrA, a novel ABC multidrug efflux pump from Stenotrophomonas maltophilia. J Antimicrob Chemother 2009; 64(4): 731-4.
[http://dx.doi.org/10.1093/jac/dkp271] [PMID: 19643774]
[116]
Lin YT, Huang YW, Liou RS, Chang YC, Yang TC. MacABCsm, an ABC-type tripartite efflux pump of Stenotrophomonas maltophilia involved in drug resistance, oxidative and envelope stress tolerances and biofilm formation. J Antimicrob Chemother 2014; 69(12): 3221-6.
[http://dx.doi.org/10.1093/jac/dku317] [PMID: 25139838]
[117]
Hu RM, Liao ST, Huang CC, Huang YW, Yang TC. An inducible fusaric acid tripartite efflux pump contributes to the fusaric acid resistance in Stenotrophomonas maltophilia. PLoS One 2012; 7(12)e51053
[http://dx.doi.org/10.1371/journal.pone.0051053] [PMID: 23236431]
[118]
Li XZ, Zhang L, Poole K. SmeC, an outer membrane multidrug efflux protein of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2002; 46(2): 333-43.
[http://dx.doi.org/10.1128/AAC.46.2.333-343.2002] [PMID: 11796339]
[119]
Lin CW, Huang YW, Hu RM, Yang TC. SmeOP-TolCSm efflux pump contributes to the multidrug resistance of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2014; 58(4): 2405-8.
[http://dx.doi.org/10.1128/AAC.01974-13] [PMID: 24395237]
[120]
Crossman LC, Gould VC, Dow JM, et al. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 2008; 9(4): R74.
[http://dx.doi.org/10.1186/gb-2008-9-4-r74] [PMID: 18419807]
[121]
Chen CH, Huang CC, Chung TC, Hu RM, Huang YW, Yang TC. Contribution of resistance-nodulation-division efflux pump operon smeU1-V-W-U2-X to multidrug resistance of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2011; 55(12): 5826-33.
[http://dx.doi.org/10.1128/AAC.00317-11] [PMID: 21930878]
[122]
Dulyayangkul P, Charoenlap N, Srijaruskul K, Mongkolsuk S, Vattanaviboon P. Major facilitator superfamily MfsA contributes to multidrug resistance in emerging nosocomial pathogen Stenotrophomonas maltophilia. J Antimicrob Chemother 2016; 71(10): 2990-1.
[http://dx.doi.org/10.1093/jac/dkw233] [PMID: 27334664]
[123]
Zhang L, Li XZ, Poole K. SmeDEF multidrug efflux pump contributes to intrinsic multidrug resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2001; 45(12): 3497-503.
[http://dx.doi.org/10.1128/AAC.45.12.3497-3503.2001] [PMID: 11709330]
[124]
Alonso A, Martínez JL. Cloning and characterization of SmeDEF, a novel multidrug efflux pump from Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2000; 44(11): 3079-86.
[http://dx.doi.org/10.1128/AAC.44.11.3079-3086.2000] [PMID: 11036026]
[125]
Althouse GC, Lu KG. Bacteriospermia in extended porcine semen. Theriogenology 2005; 63(2): 573-84.
[http://dx.doi.org/10.1016/j.theriogenology.2004.09.031] [PMID: 15626417]
[126]
Kilburn C, Rooks DJ, McCarthy AJ, Murray RD. Antimicrobial resistance in some gram-negative bacteria isolated from the bovine ejaculate. Reprod Domest Anim 2013; 48(3): 525-8.
[http://dx.doi.org/10.1111/rda.12127] [PMID: 23331295]
[127]
O’Connell D, Mruk K, Rocheleau JM, Kobertz WR. Xenopus laevis oocytes infected with multi-drug-resistant bacteria: Implications for electrical recordings. J Gen Physiol 2011; 138(2): 271-7.
[http://dx.doi.org/10.1085/jgp.201110661] [PMID: 21788613]
[128]
Johnson EH, Al-Busaidy R, Hameed MS. An outbreak of lymphadenitis associated with Stenotrophomonas (Xanthomonas) maltophilia in Omani goats. J Vet Med B Infect Dis Vet Public Health 2003; 50(2): 102-4.
[http://dx.doi.org/10.1046/j.1439-0450.2003.00643.x] [PMID: 12675904]
[129]
Macdiarmid JA, Burrell DH. Characterization of Pseudomonas maltophilia isolates from fleece rot. Appl Environ Microbiol 1986; 51(2): 346-8.
[http://dx.doi.org/10.1128/aem.51.2.346-348.1986] [PMID: 16346990]
[130]
Sánchez P, Alonso A, Martinez JL. Cloning and characterization of SmeT, a repressor of the Stenotrophomonas maltophilia multidrug efflux pump SmeDEF. Antimicrob Agents Chemother 2002; 46(11): 3386-93.
[http://dx.doi.org/10.1128/AAC.46.11.3386-3393.2002] [PMID: 12384340]
[131]
Zhao J, Liu Y, Liu Y, et al. Frequency and genetic determinants of tigecycline resistance in clinically isolated Stenotrophomonas maltophilia in Beijing, China. Front Microbiol 2018; 9: 549.
[http://dx.doi.org/10.3389/fmicb.2018.00549] [PMID: 29632524]
[132]
Zhang L, Li XZ, Poole K. Multiple antibiotic resistance in Stenotrophomonas maltophilia: Involvement of a multidrug efflux system. Antimicrob Agents Chemother 2000; 44(2): 287-93.
[http://dx.doi.org/10.1128/AAC.44.2.287-293.2000] [PMID: 10639352]
[133]
Huang TP, Wong AC. A cyclic AMP receptor protein-regulated cell-cell communication system mediates expression of a FecA homologue in Stenotrophomonas maltophilia. Appl Environ Microbiol 2007; 73(15): 5034-40.
[http://dx.doi.org/10.1128/AEM.00366-07] [PMID: 17574998]
[134]
Huedo P, Coves X, Daura X, Gibert I, Yero D. Quorum sensing signaling and quenching in the multidrug-resistant pathogen Stenotrophomonas maltophilia. Front Cell Infect Microbiol 2018; 8: 122.
[http://dx.doi.org/10.3389/fcimb.2018.00122] [PMID: 29740543]
[135]
Yero D, Huedo P, Conchillo-Solé O, et al. Genetic variants of the DSF quorum sensing system in Stenotrophomonas maltophilia influence virulence and resistance phenotypes among genotypically diverse clinical isolates. Front Microbiol 2020; 11: 1160.
[http://dx.doi.org/10.3389/fmicb.2020.01160] [PMID: 32582100]
[136]
Ryan RP, Monchy S, Cardinale M, et al. The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 2009; 7(7): 514-25.
[http://dx.doi.org/10.1038/nrmicro2163] [PMID: 19528958]
[137]
Papenfort K, Bassler BL. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 2016; 14(9): 576-88.
[http://dx.doi.org/10.1038/nrmicro.2016.89] [PMID: 27510864]
[138]
An SQ, Tang JL. The Ax21 protein influences virulence and biofilm formation in Stenotrophomonas maltophilia. Arch Microbiol 2018; 200(1): 183-7.
[http://dx.doi.org/10.1007/s00203-017-1433-7] [PMID: 28965241]
[139]
Devos S, Van Oudenhove L, Stremersch S, et al. The effect of imipenem and diffusible signaling factors on the secretion of outer membrane vesicles and associated Ax21 proteins in Stenotrophomonas maltophilia. Front Microbiol 2015; 6: 298.
[http://dx.doi.org/10.3389/fmicb.2015.00298] [PMID: 25926824]
[140]
Hu H, He J, Liu J, Yu H, Tang J, Zhang J. Role of N-Acyl-Homoserine Lactone (AHL) based quorum sensing on biofilm formation on packing media in wastewater treatment process. RSC Advances 2016; 6(14): 11128-39.
[http://dx.doi.org/10.1039/C5RA23466B]
[141]
Valle A, Bailey MJ, Whiteley AS, Manefield M. N-Acyl-l-Homoserine Lactones (AHLs) affect microbial community composition and function in activated sludge. Environ Microbiol 2004; 6(4): 424-33.
[http://dx.doi.org/10.1111/j.1462-2920.2004.00581.x] [PMID: 15008819]
[142]
Tan CH, Koh KS, Xie C, et al. Community quorum sensing signalling, and quenching: Microbial granular biofilm assembly. NPJ Biofilms Microbiomes 2015; 1(1): 1-9.
[http://dx.doi.org/10.1038/npjbiofilms.2015.6]
[143]
Venturi V. LuxR-family “solos”: Bachelor sensors/regulators of signalling molecules. Microbiology 2009.
[http://dx.doi.org/10.1099/mic.0.026849-0]
[144]
Hudaiberdiev S, Choudhary KS, Vera Alvarez R, et al. Census of solo LuxR genes in prokaryotic genomes. Front Cell Infect Microbiol 2015; 5: 20.
[http://dx.doi.org/10.3389/fcimb.2015.00020] [PMID: 25815274]
[145]
Martínez P, Huedo P, Martinez-Servat S, et al. Stenotrophomonas maltophilia responds to exogenous AHL signals through the LuxR solo SmoR (Smlt1839). Front Cell Infect Microbiol 2015; 5: 41.
[http://dx.doi.org/10.3389/fcimb.2015.00041] [PMID: 26029670]
[146]
Borovilos M, Shulman ST, Brooke JS. Role of flagella in biofilm formation by Stenotrophomonas maltophilia, abstr B2. Abstr. 55th Annual International Conference Canadian Society of Microbiologists 2005.
[147]
Travis J, Potempa J, Maeda H. Are bacterial proteinases pathogenic factors? Trends Microbiol 1995; 3(10): 405-7.
[http://dx.doi.org/10.1016/S0966-842X(00)88988-X] [PMID: 8564361]
[148]
Huang X, Liu J, Ding J, He Q, Xiong R, Zhang K. The investigation of nematocidal activity in Stenotrophomonas maltophilia G2 and characterization of a novel virulence serine protease. Can J Microbiol 2009; 55(8): 934-42.
[http://dx.doi.org/10.1139/W09-045] [PMID: 19898533]
[149]
Matsumoto K. Role of bacterial proteases in pseudomonal and serratial keratitis. Biol Chem 2004; 385(11): 1007-16.
[http://dx.doi.org/10.1515/BC.2004.131] [PMID: 15576320]
[150]
Elsner HA, Dührsen U, Hollwitz B, Kaulfers PM, Hossfeld DK. Fatal pulmonary hemorrhage in patients with acute leukemia and fulminant pneumonia caused by Stenotrophomonas maltophilia. Ann Hematol 1997; 74(4): 155-61.
[http://dx.doi.org/10.1007/s002770050275] [PMID: 9174542]
[151]
Tamura H, Yamashita S, Kusano N, et al. Fulminant hepatitis complicated by small intestine infection and massive hemorrhage. J Gastroenterol 1998; 33(3): 412-8.
[http://dx.doi.org/10.1007/s005350050105] [PMID: 9658323]
[152]
Ohkoshi Y, Ninomiya H, Mukai HY, et al. Pseudoaneurysm of the subclavian artery due to Xanthomonas pneumonia in a patient with acute myeloid leukemia: Its rupture treated by transcatheter coil embolization. Intern Med 1999; 38(8): 671-4.
[http://dx.doi.org/10.2169/internalmedicine.38.671] [PMID: 10440506]
[153]
DuMont AL, Cianciotto NP. Stenotrophomonas maltophilia serine protease StmPr1 induces matrilysis, anoikis, and protease-activated receptor 2 activation in human lung epithelial cells. Infect Immun 2017; 85(12): e00544-17.
[http://dx.doi.org/10.1128/IAI.00544-17] [PMID: 28893914]
[154]
DuMont AL, Karaba SM, Cianciotto NP, Type II. Type II secretion-dependent degradative and cytotoxic activities mediated by Stenotrophomonas maltophilia serine proteases StmPr1 and StmPr2. Infect Immun 2015; 83(10): 3825-37.
[http://dx.doi.org/10.1128/IAI.00672-15] [PMID: 26169274]
[155]
Ribitsch D, Heumann S, Karl W, et al. Extracellular serine proteases from Stenotrophomonas maltophilia: Screening, isolation and heterologous expression in E. coli. J Biotechnol 2012; 157(1): 140-7.
[http://dx.doi.org/10.1016/j.jbiotec.2011.09.025] [PMID: 21983234]
[156]
Di Rosa R, Creti R, Venditti M, et al. Relationship between biofilm formation, the Enterococcal surface protein (Esp) and gelatinase in clinical isolates of Enterococcus faecalis and Enterococcus faecium. FEMS Microbiol Lett 2006; 256(1): 145-50.
[http://dx.doi.org/10.1111/j.1574-6968.2006.00112.x] [PMID: 16487332]
[157]
Beri S, Shandil A, Garg R. Stenotrophomonas maltophilia: An emerging entity for cluster endophthalmitis. Indian J Ophthalmol 2017; 65(11): 1166-71.
[http://dx.doi.org/10.4103/ijo.IJO_314_17] [PMID: 29133644]
[158]
Thomas R, Hamat RA, Neela V. Extracellular enzyme profiling of Stenotrophomonas maltophilia clinical isolates. Virulence 2014; 5(2): 326-30.
[http://dx.doi.org/10.4161/viru.27724] [PMID: 24448556]
[159]
Rahmoune H, Lamblin G, Lafitte JJ, Galabert C, Filliat M, Roussel P. Chondroitin sulfate in sputum from patients with cystic fibrosis and chronic bronchitis. Am J Respir Cell Mol Biol 1991; 5(4): 315-20.
[http://dx.doi.org/10.1165/ajrcmb/5.4.315] [PMID: 1910815]
[160]
Kreil G. Hyaluronidases--a group of neglected enzymes. Protein Sci 1995; 4(9): 1666-9.
[http://dx.doi.org/10.1002/pro.5560040902]
[161]
Figueirêdo PM, Furumura MT, Santos AM, et al. Cytotoxic activity of clinical Stenotrophomonas maltophilia. Lett Appl Microbiol 2006; 43(4): 443-9.
[http://dx.doi.org/10.1111/j.1472-765X.2006.01965.x] [PMID: 16965377]
[162]
Bonny TS, Azmuda N, Khan SI, Birkeland NK, Rahman MZ. Virulence of environmental Stenotrophomonas maltophilia serologically cross-reacting with Shigella-specific antisera. Pak J Biol Sci 2010; 13(19): 937-45.
[http://dx.doi.org/10.3923/pjbs.2010.937.945]
[163]
García CA, Passerini De Rossi B, Alcaraz E, Vay C, Franco M. Siderophores of Stenotrophomonas maltophilia: Detection and determination of their chemical nature. Rev Argent Microbiol 2012; 44(3): 150-4.
[PMID: 23102461]
[164]
Garcia DDO, Timenetsky J, Martinez MB, Francisco W, Sinto SI, Yanaguita RM. Proteases (caseinase and elastase), hemolysins, adhesion and susceptibility to antimicrobials of Stenotrophomonas maltophilia isolates obtained from clinical specimens. Braz J Microbiol 2002; 33(2): 157-62.
[http://dx.doi.org/10.1590/S1517-83822002000200012]
[165]
Rowe GE, Welch RA. Assays of hemolytic toxins. Methods Enzymol 1994; 235: 657-67.
[http://dx.doi.org/10.1016/0076-6879(94)35179-1] [PMID: 7520121]
[166]
Neilands JB. Siderophores: Structure and function of microbial iron transport compounds. J Biol Chem 1995; 270(45): 26723-6.
[http://dx.doi.org/10.1074/jbc.270.45.26723] [PMID: 7592901]
[167]
Trifonova A, Strateva T. Stenotrophomonas maltophilia - a low-grade pathogen with numerous virulence factors. Infect Dis 2019; 51(3): 168-78.
[http://dx.doi.org/10.1080/23744235.2018.1531145] [PMID: 30422737]
[168]
O’Brien M, Davis GH. Enzymatic profile of Pseudomonas maltophilia. J Clin Microbiol 1982; 16(3): 417-21.
[http://dx.doi.org/10.1128/jcm.16.3.417-421.1982] [PMID: 6813350]
[169]
Arella M, Sylvestre M. Production of an extracellular ribonuclease by Pseudomonas maltophilia. Can J Microbiol 1979; 25(3): 321-8.
[http://dx.doi.org/10.1139/m79-051] [PMID: 36976]
[170]
von Riesen VL. Digestion of algin by Pseudomonas maltophilia and Pseudomonas putida. Appl Environ Microbiol 1980; 39(1): 92-6.
[http://dx.doi.org/10.1128/aem.39.1.92-96.1980] [PMID: 7356324]
[171]
Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303(5663): 1532-5.
[http://dx.doi.org/10.1126/science.1092385] [PMID: 15001782]
[172]
Lonon MK, Woods DE, Straus DC. The effects of purified 25-kDa lipase from a clinical isolate of Pseudomonas cepacia in the lungs of rats. Curr Microbiol 1992; 25(2): 89-93.
[http://dx.doi.org/10.1007/BF01570965] [PMID: 1283726]
[173]
Stehr F, Kretschmar M, Kröger C, Hube B, Schäfer W. Microbial lipases as virulence factors. J Mol Catal, B 2003; 22(5-6): 347-55.
[174]
Flores-Díaz M, Thelestam M, Clark GC, Titball RW, Alape-Girón A. Effects of Clostridium perfringens phospholipase C in mammalian cells. Anaerobe 2004; 10(2): 115-23.
[http://dx.doi.org/10.1016/j.anaerobe.2003.11.002] [PMID: 16701508]
[175]
Entenza JM, Moreillon P. Tigecycline in combination with other antimicrobials: A review of in vitro, animal and case report studies. Int J Antimicrob Agents 2009; 34(1): 8.e1-9.
[http://dx.doi.org/10.1016/j.ijantimicag.2008.11.006] [PMID: 19162449]
[176]
Barbier-Frebour N, Boutiba-Boubake I, Nouvello M, Lemelan J. Molecular investigation of Stenotrophomonas maltophilia isolates exhibiting rapid emergence of ticarcillin-clavulanate resistance. J Hosp Infect 2000; 45(1): 35-41.
[http://dx.doi.org/10.1053/jhin.1999.0708] [PMID: 10833341]
[177]
Farrell DJ, Sader HS, Jones RN. Antimicrobial susceptibilities of a worldwide collection of Stenotrophomonas maltophilia isolates tested against tigecycline and agents commonly used for S. maltophilia infections. Antimicrob Agents Chemother 2010; 54(6): 2735-7.
[http://dx.doi.org/10.1128/AAC.01774-09] [PMID: 20368399]
[178]
Sanschagrin F, Levesque RC. A specific peptide inhibitor of the class B metallo-beta-lactamase L-1 from Stenotrophomonas maltophilia identified using phage display. J Antimicrob Chemother 2005; 55(2): 252-5.
[http://dx.doi.org/10.1093/jac/dkh550] [PMID: 15659541]
[179]
Chang HC, Chen CR, Lin JW, et al. Isolation and characterization of novel giant Stenotrophomonas maltophilia phage phiSMA5. Appl Environ Microbiol 2005; 71(3): 1387-93.
[http://dx.doi.org/10.1128/AEM.71.3.1387-1393.2005] [PMID: 15746341]
[180]
Parkins MD, Elborn JS. Newer antibacterial agents and their potential role in cystic fibrosis pulmonary exacerbation management. J Antimicrob Chemother 2010; 65(9): 1853-61.
[http://dx.doi.org/10.1093/jac/dkq245] [PMID: 20605846]
[181]
Vartivarian S, Anaissie E, Bodey G, Sprigg H, Rolston K. A changing pattern of susceptibility of Xanthomonas maltophilia to antimicrobial agents: Implications for therapy. Antimicrob Agents Chemother 1994; 38(3): 624-7.
[http://dx.doi.org/10.1128/AAC.38.3.624] [PMID: 8203865]
[182]
Ba BB, Feghali H, Arpin C, Saux MC, Quentin C. Activities of ciprofloxacin and moxifloxacin against Stenotrophomonas maltophilia and emergence of resistant mutants in an in vitro pharmacokinetic-pharmacodynamic model. Antimicrob Agents Chemother 2004; 48(3): 946-53.
[http://dx.doi.org/10.1128/AAC.48.3.946-953.2004] [PMID: 14982788]
[183]
Gordon NC, Wareham DW. Antimicrobial activity of the green tea polyphenol (-)-epigallocatechin-3-gallate (EGCG) against clinical isolates of Stenotrophomonas maltophilia. Int J Antimicrob Agents 2010; 36(2): 129-31.
[http://dx.doi.org/10.1016/j.ijantimicag.2010.03.025] [PMID: 20472404]
[184]
Srijaruskul K, Charoenlap N, Namchaiw P, et al. Regulation by SoxR of mfsA, which encodes a major facilitator protein involved in paraquat resistance in Stenotrophomonas maltophilia. PLoS One 2015; 10(4)e0123699
[http://dx.doi.org/10.1371/journal.pone.0123699] [PMID: 25915643]
[185]
Maisetta G, Mangoni ML, Esin S, et al. In vitro bactericidal activity of the N-terminal fragment of the frog peptide esculentin-1b (Esc 1-18) in combination with conventional antibiotics against Stenotrophomonas maltophilia. Peptides 2009; 30(9): 1622-6.
[http://dx.doi.org/10.1016/j.peptides.2009.06.004] [PMID: 19520127]
[186]
Geller DE, Flume PA, Griffith DC, et al. Pharmacokinetics and safety of MP-376 (levofloxacin inhalation solution) in cystic fibrosis subjects. Antimicrob Agents Chemother 2011; 55(6): 2636-40.
[http://dx.doi.org/10.1128/AAC.01744-10] [PMID: 21444699]
[187]
Al-Hamad A, Burnie J, Upton M. Enhancement of antibiotic susceptibility of Stenotrophomonas maltophilia using a polyclonal antibody developed against an ABC multidrug efflux pump. Can J Microbiol 2011; 57(10): 820-8.
[http://dx.doi.org/10.1139/w11-076] [PMID: 21942332]
[188]
Avison MB, Higgins CS, von Heldreich CJ, Bennett PM, Walsh TR. Plasmid location and molecular heterogeneity of the L1 and L2 beta-lactamase genes of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2001; 45(2): 413-9.
[http://dx.doi.org/10.1128/AAC.45.2.413-419.2001] [PMID: 11158734]
[189]
Senol E, DesJardin J, Stark PC, Barefoot L, Snydman DR. Attributable mortality of Stenotrophomonas maltophilia bacteremia. Clin Infect Dis 2002; 34(12): 1653-6.
[http://dx.doi.org/10.1086/340707] [PMID: 12032905]
[190]
Lerouge I, Vanderleyden J. O-antigen structural variation: Mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol Rev 2002; 26(1): 17-47.
[http://dx.doi.org/10.1111/j.1574-6976.2002.tb00597.x] [PMID: 12007641]
[191]
Gröschel MI, Meehan CJ, Barilar I, et al. The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia. Nat Commun 2020; 11(1): 2044.
[http://dx.doi.org/10.1038/s41467-020-15123-0] [PMID: 32341346]
[192]
Waters V, Atenafu EG, Salazar JG, et al. Chronic Stenotrophomonas maltophilia infection and exacerbation outcomes in cystic fibrosis. J Cyst Fibros 2012; 11(1): 8-13.
[http://dx.doi.org/10.1016/j.jcf.2011.07.008]
[193]
Vidigal PG, Müsken M, Becker KA, et al. Effects of green tea compound epigallocatechin-3-gallate against Stenotrophomonas maltophilia infection and biofilm. PLoS One 2014; 9(4)e92876
[http://dx.doi.org/10.1371/journal.pone.0092876] [PMID: 24690894]
[194]
Xu G, Tang X, Shang X, et al. Identification of immunogenic outer membrane proteins and evaluation of their protective efficacy against Stenotrophomonas maltophilia. BMC Infect Dis 2018; 18(1): 347.
[http://dx.doi.org/10.1186/s12879-018-3258-7] [PMID: 30053835]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy