Antimicrobial Susceptibility and Sub-MIC Biofilm Formation of Moraxella catarrhalis Clinical Isolates under Anaerobic Conditions
Affiliation(s)
Department of Microbiology and Immunology, Midwestern University, Downers Grove, Illinois, USA.
Department of Microbiology and Immunology, Midwestern University, Downers Grove, Illinois, USA.
ABSTRACT
A medium was developed to support the anaerobic growth and antimicrobial susceptibility testing of clinical Moraxella catarrhalis isolates. The MICs of clinical Moraxella catarrhalis isolates under anaerobic conditions were, in general, decreased as compared to atmospheric or capnophilic conditions, while the MBCs for all conditions were within a 2 fold concentration dilution. Biofilm formation was affected by the presence of sub-MIC concentrations of azithromycin and the tested quinolones with the exception of levofloxacin.
A medium was developed to support the anaerobic growth and antimicrobial susceptibility testing of clinical Moraxella catarrhalis isolates. The MICs of clinical Moraxella catarrhalis isolates under anaerobic conditions were, in general, decreased as compared to atmospheric or capnophilic conditions, while the MBCs for all conditions were within a 2 fold concentration dilution. Biofilm formation was affected by the presence of sub-MIC concentrations of azithromycin and the tested quinolones with the exception of levofloxacin.
KEYWORDS
Anaerobic, Nitrate, Otitis Media, Sinusitis, Pneumonia, Biofilm, Sub-MIC, Anaerobic Respiration, Moraxella catarrhalis
Anaerobic, Nitrate, Otitis Media, Sinusitis, Pneumonia, Biofilm, Sub-MIC, Anaerobic Respiration, Moraxella catarrhalis
Cite this paper
Plotkin, B. , Hatakeyama, T. and Ma, Z. (2015) Antimicrobial Susceptibility and Sub-MIC Biofilm Formation of Moraxella catarrhalis Clinical Isolates under Anaerobic Conditions. Advances in Microbiology, 5, 244-251. doi: 10.4236/aim.2015.54022.
Plotkin, B. , Hatakeyama, T. and Ma, Z. (2015) Antimicrobial Susceptibility and Sub-MIC Biofilm Formation of Moraxella catarrhalis Clinical Isolates under Anaerobic Conditions. Advances in Microbiology, 5, 244-251. doi: 10.4236/aim.2015.54022.
References
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http://dx.doi.org/10.1146/annurev.mi.49.100195.003431 [2] Costerton, J.W., Stewart, P.S. and Greenberg, E.P. (1999) Bacterial Biofilms: A Common Cause of Persistent Infections. Science, 284, 1318-1322.
http://dx.doi.org/10.1126/science.284.5418.1318 [3] Gilbert, P., Maira-Litran, T., McBain, A., Rickard, A. and Whyte, F. (2002) The Physiology and Collective Recalcitrance of Microbial Biofilm Communities. Advances in Microbial Physiology, 46, 202-256.
http://dx.doi.org/10.1016/S0065-2911(02)46005-5 [4] Dongari-Bagtzoglou, A. (2008) Pathogenesis of Mucosal Biofilm Infections: Challenges and Progress. Expert Review of Anti-Infective Therapy, 6, 201-208.
http://dx.doi.org/10.1586/14787210.6.2.201 [5] Lewis, K. (2001) Riddle of Biofilm Resistance. Antimicrob Agents Chemother, 45, 999-1007.
http://dx.doi.org/10.1128/AAC.45.4.999-1007.2001 [6] Wise, R., Hart, T., Cars, O., Streulens, M., Helmuth, R., Huovinen, P. and Sprenger, M. (1998) Antimicrobial Resistance. BMJ, 317, 609-610.
http://dx.doi.org/10.1136/bmj.317.7159.609 [7] Farzam, F. and Plotkin, B.J. (2001) Effect of Sub-MICs of Antibiotics on the Hydrophobicity and Production of Acidic Polysaccharide by Vibrio vulnificus. Chemotherapy, 47, 184-193.
http://dx.doi.org/10.1159/000063220 [8] Pinheiro, L., Brito, C.I., Pereira, V.C., de Oliveira, A., Camargo, C.H. and da Cunha, M. (2014) Reduced Susceptibility to Vancomycin and Biofilm Formation in Methicillin-Resistant Staphylococcus epidermidis Isolated from Blood Cultures. Memórias do Instituto Oswaldo Cruz, 109, 871-878.
http://dx.doi.org/10.1590/0074-0276140120 [9] Wojnicz, D. (2007) The Influence of Subinhibitory Concentrations of Antibiotics on the Bacterial Adhesion. Advances in Clinical and Experimental Medicine, 16, 141-148. [10] Lau, D. and Plotkin, B. (2013) Antimicrobial and Biofilm Effects of Herbs Used in Traditional Chinese Medicine. Natural Product Communications, 8, 1617-1620. [11] Borriello, G., Werner, E., Roe, F., Kim, A., Ehrlich, G. and Stewart, P. (2004) Oxygen Limitation Contributes to Antibiotic Tolerance of Pseudomonas aeruginosa in Biofilms. Antimicrobial Agents and Chemotherapy, 48, 2659-2664.
http://dx.doi.org/10.1128/AAC.48.7.2659-2664.2004 [12] Murphy, T. and Parameswaran, G. (2009) Moraxella catarrhalis, a Human Respiratory Tract Pathogen. Clinical Infectious Diseases, 49, 124-131.
http://dx.doi.org/10.1086/599375 [13] Daly, K.A., Hoffman, H.J., Kvaerner, K.J., Casselbrant, M.L., Homoe, P. and Rovers, M.M. (2010) Epidemiology, Natural History, and Risk Factors: Panel Report from the Ninth International Research Conference on Otitis Media. International Journal of Pediatric Otorhinolaryngology, 74, 231-240.
http://dx.doi.org/10.1016/j.ijporl.2009.09.006 [14] Leibovitz, E., Broides, A., Greenberg, D. and Newman, N. (2010) Current Management of Pediatric Acute Otitis Media. Expert Review of Anti-Infective Therapy, 8, 151-161.
http://dx.doi.org/10.1586/eri.09.112 [15] Thornton, R.B., Wiertsema, S.P., Kirkham, L.A.S., Rigby, P.J., Vijayasekaran, S., Coates, H.L. and Richmond, P.C. (2013) Neutrophil Extracellular Traps and Bacterial Biofilms in Middle Ear Effusion of Children with Recurrent Acute Otitis Media—A Potential Treatment Target. PLoS ONE, 8, e53837. http://dx.doi.org/10.1371/journal.pone.0053837 [16] Pelton, S.I. and Leibovitz, E. (2009) Recent Advances in Otitis Media. Pediatric Infectious Disease Journal, 28, S133-S137.
http://dx.doi.org/10.1097/INF.0b013e3181b6d81a [17] Parameswaran, G.I. and Murphy, T.F. (2009) Chronic Obstructive Pulmonary Disease. Role of Bacteria and Updated Guide to Antibacterial Selection in the Older Patient. Drugs & Aging, 26, 985-995.
http://dx.doi.org/10.2165/11315700-000000000-00000 [18] Takahashi, M., Niwa, H. and Yanagita, N. (1990) PO2 Levels in Middle Ear Effusions and Middle Ear Mucosa. Acta Oto-Laryngologica, 110, 39-42.
http://dx.doi.org/10.3109/00016489009124807 [19] Kostova, M., Myers, C., Beck, T., Plotkin, B., Green, J., Boshoff, H., Barry III, C.E., Deschamps, J. and Konaklieva, M. (2011) C4-Alkylthiols with Activity against Moraxella catarrhalis and Mycobacterium tuberculosis. Bioorganic & Medicinal Chemistry, 19, 6842-6852.
http://dx.doi.org/10.1016/j.bmc.2011.09.030 [20] Brook, I. (2005) Microbiology and Antimicrobial Management of Sinusitis. Journal of Laryngology & Otology, 119, 251-258.
http://dx.doi.org/10.1258/0022215054020304 [21] Kirby, D., Raino, C., Rabor Jr., S.F., Wasson, C. and Plotkin, B. (2012) Semi-Automated Method for Multi-Tasking Measurement of Microbial Growth, Capsule, and Biofilm Formation. Advances in Microbiology, 2, 623-628.
http://dx.doi.org/10.4236/aim.2012.24081 [22] Wang, W., Kinkel, T., Martens-Habbena, W., Stahl, D.A., Fang, F.C. and Hansen, E.J. (2011) The Moraxella catarrhalis Nitric Oxide Reductase Is Essential for Nitric Oxide Detoxification. Journal of Bacteriology, 193, 2804-2813.
http://dx.doi.org/10.1128/JB.00139-11 [23] Wang, W., Reitzer, L., Rasko, D., Pearson, M., Blick, R., Laurence, C. and Hansen, E. (2007) Metabolic Analysis of Moraxella catarrhalis and the Effect of Selected in Vitro Growth Conditions on Global Gene Expression. Infection and Immunity, 75, 4959-4971.
http://dx.doi.org/10.1128/IAI.00073-07 [24] Fux, C., Shirtliff, M., Stoodley, P. and Costerton, J. (2005) Can Laboratory Reference Strains Mirror “Real-World” Pathogenesis? Trends in Microbiology, 13, 58-63.
http://dx.doi.org/10.1016/j.tim.2004.11.001 [25] Brook, I. (2006) Bacteriology of Chronic Sinusitis and Acute Exacerbation of Chronic Sinusitis. JAMA Otolaryngology-Head & Neck Surgery, 132, 1099-1101.
http://dx.doi.org/10.1001/archotol.132.10.1099 [26] Hoban, D.J., Doern, G.V., Fluit, A.C., Roussel-Delvallez, M. and Jones, R.N. (2001) Worldwide Prevalence of Antimicrobial Resistance in Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis in the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clinical Infectious Diseases, 32, S81-S93.
http://dx.doi.org/10.1086/320181 [27] Manfredi, R., Nanetti, A., Valentini, R. and Chiodo, F. (2000) Moraxella catarrhalis Pneumonia during HIV Disease. Journal of Chemotherapy, 12, 406-411.
http://dx.doi.org/10.1179/joc.2000.12.5.406 [28] Marchisio, P., Ghisalberti, E., Fusi, M., Baggi, E., Ragazzi, M. and Dusi, E. (2007) Paranasal Sinuses and Middle Ear Infections: What Do They Have in Common? Pediatric Allergy and Immunology, 18, 31-34.
http://dx.doi.org/10.1111/j.1399-3038.2007.00630.x [29] Falsetta, M., Steichen, C., McEwan, A., Cho, C., Ketterer, M., Shao, J., Hunt, J., Jennings, M. and Apicella, M. (2011) The Composition and Metabolic Phenotype of Neisseria gonorrhoeae Biofilms. Frontiers in Microbiology, 2, 75.
http://dx.doi.org/10.3389/fmicb.2011.00075 [30] Kofoed, M., Nielsen, D., Revsbech, N. and Schramm, A. (2012) Fluorescence in Situ Hybridization (FISH) Detection of Nitrite Reductase Transcripts (nirS mRNA) in Pseudomonas stutzeri Biofilms Relative to a Microscale Oxygen Gradient. Systematic and Applied Microbiology, 35, 513-517.
http://dx.doi.org/10.1016/j.syapm.2011.12.001 [31] John, E., Russell, P., Nam, B., Jinn, T. and Jung, T. (2001) Concentration of Nitric Oxide Metabolites in Middle Ear Effusion. International Journal of Pediatric Otorhinolaryngology, 60, 55-58.
http://dx.doi.org/10.1016/S0165-5876(01)00509-2 [32] Hamad, M., Austin, C., Stewart, A., Higgins, M., Vázquez-Torres, A. and Voskuil, M. (2011) Adaptation and Antibiotic Tolerance of Anaerobic Burkholderia pseudomallei. Antimicrobial Agents and Chemotherapy, 55, 3313-3323.
http://dx.doi.org/10.1128/AAC.00953-10 [33] Clinical and Laboratory Standards Institute, Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard. M07-A8. 2009. [34] Hoopman, T.C., Liu, W., Joslin, S.N., Pybus, C., Sedillo, J.L., Labandeira-Rey, M., Laurence, C.A., Wang, W., Richardson, J.A., Bakaletz, L.O. and Hansen, E.J. (2012) Use of the Chinchilla Model for Nasopharyngeal Colonization to Study Gene Expression by Moraxella catarrhalis. Infection and Immunity, 80, 982-995.
http://dx.doi.org/10.1128/IAI.05918-11 [35] Pearson, M., Laurence, C., Guinn, S. and Hansen, E. (2006) Biofilm Formation by Moraxella catarrhalis in Vitro: Roles of the UspA1 Adhesin and the Hag Hemagglutinin. Infection and Immunity, 74, 1588-1596.
http://dx.doi.org/10.1128/IAI.74.3.1588-1596.2006
[1] Costerton, J., Lewandowski, Z., Caldwell, D., Korber, D. and Lappin-Scott, H. (1995) Microbial Biofilms. Annual Review of Microbiology, 49, 711-745.
http://dx.doi.org/10.1146/annurev.mi.49.100195.003431 [2] Costerton, J.W., Stewart, P.S. and Greenberg, E.P. (1999) Bacterial Biofilms: A Common Cause of Persistent Infections. Science, 284, 1318-1322.
http://dx.doi.org/10.1126/science.284.5418.1318 [3] Gilbert, P., Maira-Litran, T., McBain, A., Rickard, A. and Whyte, F. (2002) The Physiology and Collective Recalcitrance of Microbial Biofilm Communities. Advances in Microbial Physiology, 46, 202-256.
http://dx.doi.org/10.1016/S0065-2911(02)46005-5 [4] Dongari-Bagtzoglou, A. (2008) Pathogenesis of Mucosal Biofilm Infections: Challenges and Progress. Expert Review of Anti-Infective Therapy, 6, 201-208.
http://dx.doi.org/10.1586/14787210.6.2.201 [5] Lewis, K. (2001) Riddle of Biofilm Resistance. Antimicrob Agents Chemother, 45, 999-1007.
http://dx.doi.org/10.1128/AAC.45.4.999-1007.2001 [6] Wise, R., Hart, T., Cars, O., Streulens, M., Helmuth, R., Huovinen, P. and Sprenger, M. (1998) Antimicrobial Resistance. BMJ, 317, 609-610.
http://dx.doi.org/10.1136/bmj.317.7159.609 [7] Farzam, F. and Plotkin, B.J. (2001) Effect of Sub-MICs of Antibiotics on the Hydrophobicity and Production of Acidic Polysaccharide by Vibrio vulnificus. Chemotherapy, 47, 184-193.
http://dx.doi.org/10.1159/000063220 [8] Pinheiro, L., Brito, C.I., Pereira, V.C., de Oliveira, A., Camargo, C.H. and da Cunha, M. (2014) Reduced Susceptibility to Vancomycin and Biofilm Formation in Methicillin-Resistant Staphylococcus epidermidis Isolated from Blood Cultures. Memórias do Instituto Oswaldo Cruz, 109, 871-878.
http://dx.doi.org/10.1590/0074-0276140120 [9] Wojnicz, D. (2007) The Influence of Subinhibitory Concentrations of Antibiotics on the Bacterial Adhesion. Advances in Clinical and Experimental Medicine, 16, 141-148. [10] Lau, D. and Plotkin, B. (2013) Antimicrobial and Biofilm Effects of Herbs Used in Traditional Chinese Medicine. Natural Product Communications, 8, 1617-1620. [11] Borriello, G., Werner, E., Roe, F., Kim, A., Ehrlich, G. and Stewart, P. (2004) Oxygen Limitation Contributes to Antibiotic Tolerance of Pseudomonas aeruginosa in Biofilms. Antimicrobial Agents and Chemotherapy, 48, 2659-2664.
http://dx.doi.org/10.1128/AAC.48.7.2659-2664.2004 [12] Murphy, T. and Parameswaran, G. (2009) Moraxella catarrhalis, a Human Respiratory Tract Pathogen. Clinical Infectious Diseases, 49, 124-131.
http://dx.doi.org/10.1086/599375 [13] Daly, K.A., Hoffman, H.J., Kvaerner, K.J., Casselbrant, M.L., Homoe, P. and Rovers, M.M. (2010) Epidemiology, Natural History, and Risk Factors: Panel Report from the Ninth International Research Conference on Otitis Media. International Journal of Pediatric Otorhinolaryngology, 74, 231-240.
http://dx.doi.org/10.1016/j.ijporl.2009.09.006 [14] Leibovitz, E., Broides, A., Greenberg, D. and Newman, N. (2010) Current Management of Pediatric Acute Otitis Media. Expert Review of Anti-Infective Therapy, 8, 151-161.
http://dx.doi.org/10.1586/eri.09.112 [15] Thornton, R.B., Wiertsema, S.P., Kirkham, L.A.S., Rigby, P.J., Vijayasekaran, S., Coates, H.L. and Richmond, P.C. (2013) Neutrophil Extracellular Traps and Bacterial Biofilms in Middle Ear Effusion of Children with Recurrent Acute Otitis Media—A Potential Treatment Target. PLoS ONE, 8, e53837. http://dx.doi.org/10.1371/journal.pone.0053837 [16] Pelton, S.I. and Leibovitz, E. (2009) Recent Advances in Otitis Media. Pediatric Infectious Disease Journal, 28, S133-S137.
http://dx.doi.org/10.1097/INF.0b013e3181b6d81a [17] Parameswaran, G.I. and Murphy, T.F. (2009) Chronic Obstructive Pulmonary Disease. Role of Bacteria and Updated Guide to Antibacterial Selection in the Older Patient. Drugs & Aging, 26, 985-995.
http://dx.doi.org/10.2165/11315700-000000000-00000 [18] Takahashi, M., Niwa, H. and Yanagita, N. (1990) PO2 Levels in Middle Ear Effusions and Middle Ear Mucosa. Acta Oto-Laryngologica, 110, 39-42.
http://dx.doi.org/10.3109/00016489009124807 [19] Kostova, M., Myers, C., Beck, T., Plotkin, B., Green, J., Boshoff, H., Barry III, C.E., Deschamps, J. and Konaklieva, M. (2011) C4-Alkylthiols with Activity against Moraxella catarrhalis and Mycobacterium tuberculosis. Bioorganic & Medicinal Chemistry, 19, 6842-6852.
http://dx.doi.org/10.1016/j.bmc.2011.09.030 [20] Brook, I. (2005) Microbiology and Antimicrobial Management of Sinusitis. Journal of Laryngology & Otology, 119, 251-258.
http://dx.doi.org/10.1258/0022215054020304 [21] Kirby, D., Raino, C., Rabor Jr., S.F., Wasson, C. and Plotkin, B. (2012) Semi-Automated Method for Multi-Tasking Measurement of Microbial Growth, Capsule, and Biofilm Formation. Advances in Microbiology, 2, 623-628.
http://dx.doi.org/10.4236/aim.2012.24081 [22] Wang, W., Kinkel, T., Martens-Habbena, W., Stahl, D.A., Fang, F.C. and Hansen, E.J. (2011) The Moraxella catarrhalis Nitric Oxide Reductase Is Essential for Nitric Oxide Detoxification. Journal of Bacteriology, 193, 2804-2813.
http://dx.doi.org/10.1128/JB.00139-11 [23] Wang, W., Reitzer, L., Rasko, D., Pearson, M., Blick, R., Laurence, C. and Hansen, E. (2007) Metabolic Analysis of Moraxella catarrhalis and the Effect of Selected in Vitro Growth Conditions on Global Gene Expression. Infection and Immunity, 75, 4959-4971.
http://dx.doi.org/10.1128/IAI.00073-07 [24] Fux, C., Shirtliff, M., Stoodley, P. and Costerton, J. (2005) Can Laboratory Reference Strains Mirror “Real-World” Pathogenesis? Trends in Microbiology, 13, 58-63.
http://dx.doi.org/10.1016/j.tim.2004.11.001 [25] Brook, I. (2006) Bacteriology of Chronic Sinusitis and Acute Exacerbation of Chronic Sinusitis. JAMA Otolaryngology-Head & Neck Surgery, 132, 1099-1101.
http://dx.doi.org/10.1001/archotol.132.10.1099 [26] Hoban, D.J., Doern, G.V., Fluit, A.C., Roussel-Delvallez, M. and Jones, R.N. (2001) Worldwide Prevalence of Antimicrobial Resistance in Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis in the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clinical Infectious Diseases, 32, S81-S93.
http://dx.doi.org/10.1086/320181 [27] Manfredi, R., Nanetti, A., Valentini, R. and Chiodo, F. (2000) Moraxella catarrhalis Pneumonia during HIV Disease. Journal of Chemotherapy, 12, 406-411.
http://dx.doi.org/10.1179/joc.2000.12.5.406 [28] Marchisio, P., Ghisalberti, E., Fusi, M., Baggi, E., Ragazzi, M. and Dusi, E. (2007) Paranasal Sinuses and Middle Ear Infections: What Do They Have in Common? Pediatric Allergy and Immunology, 18, 31-34.
http://dx.doi.org/10.1111/j.1399-3038.2007.00630.x [29] Falsetta, M., Steichen, C., McEwan, A., Cho, C., Ketterer, M., Shao, J., Hunt, J., Jennings, M. and Apicella, M. (2011) The Composition and Metabolic Phenotype of Neisseria gonorrhoeae Biofilms. Frontiers in Microbiology, 2, 75.
http://dx.doi.org/10.3389/fmicb.2011.00075 [30] Kofoed, M., Nielsen, D., Revsbech, N. and Schramm, A. (2012) Fluorescence in Situ Hybridization (FISH) Detection of Nitrite Reductase Transcripts (nirS mRNA) in Pseudomonas stutzeri Biofilms Relative to a Microscale Oxygen Gradient. Systematic and Applied Microbiology, 35, 513-517.
http://dx.doi.org/10.1016/j.syapm.2011.12.001 [31] John, E., Russell, P., Nam, B., Jinn, T. and Jung, T. (2001) Concentration of Nitric Oxide Metabolites in Middle Ear Effusion. International Journal of Pediatric Otorhinolaryngology, 60, 55-58.
http://dx.doi.org/10.1016/S0165-5876(01)00509-2 [32] Hamad, M., Austin, C., Stewart, A., Higgins, M., Vázquez-Torres, A. and Voskuil, M. (2011) Adaptation and Antibiotic Tolerance of Anaerobic Burkholderia pseudomallei. Antimicrobial Agents and Chemotherapy, 55, 3313-3323.
http://dx.doi.org/10.1128/AAC.00953-10 [33] Clinical and Laboratory Standards Institute, Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard. M07-A8. 2009. [34] Hoopman, T.C., Liu, W., Joslin, S.N., Pybus, C., Sedillo, J.L., Labandeira-Rey, M., Laurence, C.A., Wang, W., Richardson, J.A., Bakaletz, L.O. and Hansen, E.J. (2012) Use of the Chinchilla Model for Nasopharyngeal Colonization to Study Gene Expression by Moraxella catarrhalis. Infection and Immunity, 80, 982-995.
http://dx.doi.org/10.1128/IAI.05918-11 [35] Pearson, M., Laurence, C., Guinn, S. and Hansen, E. (2006) Biofilm Formation by Moraxella catarrhalis in Vitro: Roles of the UspA1 Adhesin and the Hag Hemagglutinin. Infection and Immunity, 74, 1588-1596.
http://dx.doi.org/10.1128/IAI.74.3.1588-1596.2006