Commensal Staphylococcus isolates from the nasal cavity of community older adults in Valencia (Spain) and their resistance to methicillin and other antibiotics
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Nov 8, 2019
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Gozalbo Falomir, D., Rico Vidal, H., & Falomir Llorens, M. P. (2019). Commensal Staphylococcus isolates from the nasal cavity of community older adults in Valencia (Spain) and their resistance to methicillin and other antibiotics. European Journal of Health Research, 5(2), 145–158. https://doi.org/10.30552/ejhr.v5i2.185
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Commensal Staphylococcus isolates from the nasal cavity of community older adults in Valencia (Spain) and their resistance to methicillin and other antibiotics
Main Article Content
Abstract
Methicillin-resistant Staphylococcus aureus strains (MRSA) have been gradually disseminated worldwide, causing nosocomial and community-acquired infections, and healthy carriers of commensal MRSA constitute a reservoir of the pathogen. Other Staphylococcus species (coagulase-negative, CoNS) colonize animals and humans and include also methicillin-resistant strains (MRCoNS). Here we have determined the prevalence of S. aureus and CoNS species in the nasal cavity of community healthy older adults (n= 27, average age: 63.7 years) and their resistance to methicillin and other antibiotics. A total of 35 Staphylococcus isolates were obtained. All individuals (100%) were carriers of at least one Staphylococcus strain; 15% of subjects were S. aureus carriers, and eight subjects (30%) carried two strains. Prevalence of resistance to methicillin was 25% and 35% for S. aureus and CoNS isolates, respectively. Most isolates were resistant to penicillin G (90%) and clarithromycin (45%). Other resistances were less frequent (rifampicin, tetracycline, fosfomycin, ciprofloxacin), and no resistant isolates to chloramphenicol or vancomycin were found. Multiresistant isolates to three or four chemotherapeutic agents were detected (20% of isolates). These results suggest that the nasal cavity of healthy adults may represent an ecological niche for the transfer of resistant determinants between staphylococcal species, and point out that epidemiological surveillance of commensal MRSA carriers should extended also to MRCoNS carriers.
References
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Methicillin-resistent coagulase-negative staphylococci in the community: high homology
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Microbiology Reviews, 27(4), 870-926. doi:10.1128/CMR.00109-13
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of Valencia (Spain). Journal of Microbiology, Immunology and Infection, 47, 162-163.
doi:10.1016/j.jmii.2013.05.009
Falomir, M.P., Jávega, A., Rico, H., and Gozalbo, D. (2018). Nasal isolates of comensal
Staphylococcus aureus and non-aureus species from healthy young adults in Valencia
(Spain) and their resistance to chemotherapeutic agents. Annals of Epidemiology and
Public Health, 1, 1004. doi:10.33582/2639-4391/1004
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Staphylococcus aureus in the United States, 2001-2004. Journal of Infectious Diseases,
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Hanssen, A.M., Kjeldsen, G., and Sollid, J.U. (2004). Local variants of staphylococcal cassette
chromosome mec in sporadic methicillin-resistant Staphylococcus aureus and
methicillin-resistant coagulase-negative staphylococci: evidence of horizontal gene
transfer? Antimicrobial Agents and Chemotherapy, 48, 285-296.
doi:10.1128/AAC.48.1.285-296.2004
Hiramatsu, K., Katayama, Y., Matsuo, M., Sasaki, T., Morimoto, Y, Sekiguchi, A., and Baba, T.
(2014). Multi-drug-resistant Staphylococcus aureus and future chemotehrapy. Journal of
Infection and Chemotherapy, 20, 593-601. doi:10.1007/s00467-014-2955-8
Kadlec, K., and Schwarz, S. (2012). Antimicrobial resistance of Staphylococcus
pseudointermedius. Veterinary Dermatology, 23(4), 276-282. doi:10.1111/j.1365-
3164.2012.01056.x
Krismer, B., Weidenmaier, C., Zipperer, A., and Peschel, A. (2017). The commensal lifestyle of
Staphylococcus aureus and its interactions with the nasal microbiota. Nature Reviews
Microbiology, 15(11), 675-687. doi:10.1038/nrmicro.2017.104
Lakhundi, S., and Zhang, K. (2018). Methicillin-resistant Staphylococcus aureus: molecular
characterization, evolution, and epidemiology. Clinical Microbiology Reviews, 31(4),
pii: e00020-18. doi:10.1128/CMR.00020-18
Miller, J.G., and Kaplan, S.L. (2009). Staphylococcus aureus: a community pathogen. Infectious
Disease Clinics of North America, 23, 35-52. doi:10.1016/j.idc.2008.10.002
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doi:10.1111/j.1462-5822.2012.01832.x
Pomba, C., Rantala, M., Greko, C., Baptiste, K.E., Catry, B., van Duijkeren, E.,… Törneke, K.
(2017). Public health risk of antimicrobial resistance transfer from companion animals.
Journal of Antimicrobial Chemotherapy, 72(4), 957-968. doi:10.1093/jac/dkw481
Pujol, M., and Limón, E. (2013). General epidemiology of nosocomial infections. Surveillance
systems and programs. Enfermedades Infecciosas y Microbiología Clínica, 31(2), 108-
113. doi:10.1016/j.eimc.2013.01.001
Ruscher, C., Lubke-Beckeer. A., Wlekinsli, C.G., Soba, A., Wieler, L.H., and Walther, B. (2009).
Prevalence of methicillin-resistant Staphylococcus pseudointermedius isolated from
clinical samples of companion animals and equidaes. Veterinary Microbiology, 136,
197-201. doi:10.1016/j.vetmic.2008.10.023
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immune system. Current Opinion in Immunology, 22, 507-513.
doi:10.1016/j.coi.2010.05.003
Sievert, D.M., Ricks, P., Edwards, J.R., Schneider, A., Patel, J., Srinivasan, A., … Fridkin, S.
(2013). Antimicrobial-resistant pathogens associated with healthcare-associated
infections: summary of data reported to the National Healthcare Safety Network at the
centers for disease control and prevention, 2009-2010. Infection Control and Hospital
Epidemiology, 34, 1-14. doi:10.1086/668770
Teira, R., Teira, A., Campo, A.B., and de Benito, I. (2013). Prevalence of nasopharyngeal
colonization by methicillin-resistent Staphylococcus aureus in a population of high
school students in Torrelavega (Spain). Enfermedades Infecciosas y Microbiología
Clínica, 31(5), 349. doi:10.1016/j.eimc.2012.10.006
Tong, S.Y.C., Davis, J.S., Eichemberger, E., Holland, T.L., and Fowler, V.C. Jr. (2015).
Staphylococcus aureus infections: epidemiology, pathophysiology, clinical
manifestations, and management. Clinical Microbiology Reviews, 28, 603-661.
doi:10.1128/CMR.00134-14
Van Bijnen, E.M.E., Paget, J., de Lange-de Klerk, E.S.M., den Heijer, C.D.J., Versporten, A.,
Stobberingh, E.E.,… Schellevis, F.G. (2015). Antibiotic exposure and other risk factors
for antimicrobial resistance in nasal commensal Staphylococcus aureus: an ecological
study in 8 european countries. PLoS ONE, 10(8), e0135093.
doi:10.1371/journal.pone.0135094
Vindel, A., Trincado, P., Cuevas, O., Ballesteros, C, Bouza, E., and Cercenado, E. (2014).
Molecular epidemiology of community-associated methicillin resistant Staphylococcus
aureus in Spain: 2004-2012. Journal of Antimicrobial Chemotherapy, 69, 2913-2919.
doi:10.1093/jac/dku232
Wang, H.K., Huang, C.Y., Chen, C.J., and Huang, Y.C. (2017). Nasal Staphylococcus aureus
carriage among college student athletes in northern Taiwan. Journal of Microbiology,
Immunology and Infection, 50, 537-540. doi:10.1016/j.jmii.2016.11.005
Weidenmaier, C., Goerke, C., and Wolz, C. (2012). Staphylococcus aureus determinants for nasal
colonization. Trends in Microbiology, 20, 243-250. doi:10.1016/j.tim.2012.03.004
Wertheim, H.F., Vos, M.C., Ott, A., van Belkum, A., Voss, A., Kluytmans, J.A.,… Verbrugh,
H.A. (2004). Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in
nasal carriers versus non-carriers. Lancet, 364, 703.705. doi:10.1016/S0140-
6736(04)16897-9
aureus enterotoxins. Toxins, 2, 1751-1773. doi:10.3390/toxins2071751
Baquero, F. (2012). Metagenomic epidemiology: a public health need for the control of
antimicrobial resistance. Clinical Microbiology and Infection, 18(Suppl. 4), 67-73.
doi:10.1111/j.1469-0691.2012.03860.x
Barbier, F., Ruppé, E., Hernandez, D., Lebaux, D., Francois, P., Felix, B,… Ruimy, R. (2010).
Methicillin-resistent coagulase-negative staphylococci in the community: high homology
of SSCmec IVa between Staphylococcus epidermidis and major clones of methicillinresistant Staphylococcus aureus. The Journal of Infectious Diseases, 202(2), 270-281.
doi:10.1086/653483
Becker, A., Heilmann, C., and Peters, G. (2014). Coagulase-negative staphylococci. Clinical
Microbiology Reviews, 27(4), 870-926. doi:10.1128/CMR.00109-13
Bond, R., and Loeffler, A. (2012). What’s happened to Staphylococcus intermedius? Taxonomic
emergence of multi-drug resistance. Journal of Small Animals Practice, 53(3), 147-154.
doi:10.1111/j.1748-5827.2011.01165.x
Cercenado, E. (2016). Epidemiology of the infection by resistant Gram-positive microorganisms.
Revista Española de Quimioterapia, 26(Suppl. 1), 6-9.
Cuevas, O., Cercenado, E., Vindel, A., Guinea, J., Sánchez-Conde, M., Sánchez-Somolinos, M.,
and Bouza, E. (2004). Evolution of the antimicrobial resistance of Staphylococcus spp.
in Spain: five nationwide prevalence studies, 1986 to 2002. Antimicrobial Agents and
Chemotherapy, 48(11), 4240-4245. doi:10.1128/AAC.48.11.4240-4245.2004
Couto, N., Belas, A., Kadlec, K., Schwarz, S., and Pomba, C. (2015). Clonal diversity, virulence
patterns and antimicrobial and biocide susceptibility among human, animal and
environmental MRSA in Portugal. Journal of Antimicrobial Chemotherapy, 70, 2483-
2487. doi:10.1093/jac/dkv141
Doulgeraki, A.I., Di Ciccio, P., Ianeri, A., and Nychas, G.J.E. (2017). Methicillin-resistant foodrelated Staphylococcus aureus: a review of current knowledge and biofilm formation for
future studies and applications. Research in Microbiology, 168, 1-15.
doi:10.1016/j.resmic.2016.08.001
Dulon, M., Haamann, F., Peters, C., Schablon, A., and Nienhaus, A (2011). MRSA prevalence in
European healthcare settings: a review. BMC Infectious Diseases, 11, 138-151.
doi:10.1186/1471-2334-11-138
EPINE-EPPS (2017). Estudio de prevalencia de las infecciones nosocomiales en España. Madrid:
Sociedad Española de Medicina Preventiva, Salud Pública e Higiene.
Falomir, M.P., Gozalbo, D., and Rico, H. (2014). Occurrence of methicillin-resistant
Staphylococcus aureus in the nasal cavity of healthy volunteer students of the University
of Valencia (Spain). Journal of Microbiology, Immunology and Infection, 47, 162-163.
doi:10.1016/j.jmii.2013.05.009
Falomir, M.P., Jávega, A., Rico, H., and Gozalbo, D. (2018). Nasal isolates of comensal
Staphylococcus aureus and non-aureus species from healthy young adults in Valencia
(Spain) and their resistance to chemotherapeutic agents. Annals of Epidemiology and
Public Health, 1, 1004. doi:10.33582/2639-4391/1004
Fisher, E.L., Otto, M., and Cheung, G.Y.C. (2018). Basis of virulence in enterotoxin-mediated
staphylococcal food poisoning. Frontiers in Microbiology, 9, 436.
doi:10.3389/fmicb.2018.00436
Galán-Sánchez, F., Pérez-Eslava, M., Machuca, J., Trujillo-Soto, T., Arca.Suarez, J., and
Rodríguez-Iglesias, M. (2019). Staphylococcus aureus carriage in older populations in
community residential care homes: prevalence and molecular characterization of MRSA
isolates. Enfermedades Infecciosas y Microbiología Clínica, 37(3), 172-175.
doi:10.1016/j.eimc.2018.05.011
Gardella, N., Murzicato, S., Di Gregorio, S., Cuirolo, A., Desse, J., Crudo, F,… Mollerach, M.
(2011). Prevalence and characterization of methicillin-resistant Staphylococcus aureus
among healthy children in a city of Argentina. Infection, Genetics and Evolution, 11(5),
1066-1071. doi:10.1016/j.meegid.2011.03.019
Gorwitz, R.J., Kruszon-Moran, D., McAllister, S.K., McQuillan, G., McDougal, L.K., Fosheim,
G.E.,… Kuehnert, M.J. (2008). Changes in the prevalence of nasal colonization with
Staphylococcus aureus in the United States, 2001-2004. Journal of Infectious Diseases,
197(9), 1226-1234. doi:10.1086/533494
Hanssen, A.M., Kjeldsen, G., and Sollid, J.U. (2004). Local variants of staphylococcal cassette
chromosome mec in sporadic methicillin-resistant Staphylococcus aureus and
methicillin-resistant coagulase-negative staphylococci: evidence of horizontal gene
transfer? Antimicrobial Agents and Chemotherapy, 48, 285-296.
doi:10.1128/AAC.48.1.285-296.2004
Hiramatsu, K., Katayama, Y., Matsuo, M., Sasaki, T., Morimoto, Y, Sekiguchi, A., and Baba, T.
(2014). Multi-drug-resistant Staphylococcus aureus and future chemotehrapy. Journal of
Infection and Chemotherapy, 20, 593-601. doi:10.1007/s00467-014-2955-8
Kadlec, K., and Schwarz, S. (2012). Antimicrobial resistance of Staphylococcus
pseudointermedius. Veterinary Dermatology, 23(4), 276-282. doi:10.1111/j.1365-
3164.2012.01056.x
Krismer, B., Weidenmaier, C., Zipperer, A., and Peschel, A. (2017). The commensal lifestyle of
Staphylococcus aureus and its interactions with the nasal microbiota. Nature Reviews
Microbiology, 15(11), 675-687. doi:10.1038/nrmicro.2017.104
Lakhundi, S., and Zhang, K. (2018). Methicillin-resistant Staphylococcus aureus: molecular
characterization, evolution, and epidemiology. Clinical Microbiology Reviews, 31(4),
pii: e00020-18. doi:10.1128/CMR.00020-18
Miller, J.G., and Kaplan, S.L. (2009). Staphylococcus aureus: a community pathogen. Infectious
Disease Clinics of North America, 23, 35-52. doi:10.1016/j.idc.2008.10.002
Otto, M. (2012). MRSA virulence and spread. Cellular Microbiology, 14, 1513-1521.
doi:10.1111/j.1462-5822.2012.01832.x
Pomba, C., Rantala, M., Greko, C., Baptiste, K.E., Catry, B., van Duijkeren, E.,… Törneke, K.
(2017). Public health risk of antimicrobial resistance transfer from companion animals.
Journal of Antimicrobial Chemotherapy, 72(4), 957-968. doi:10.1093/jac/dkw481
Pujol, M., and Limón, E. (2013). General epidemiology of nosocomial infections. Surveillance
systems and programs. Enfermedades Infecciosas y Microbiología Clínica, 31(2), 108-
113. doi:10.1016/j.eimc.2013.01.001
Ruscher, C., Lubke-Beckeer. A., Wlekinsli, C.G., Soba, A., Wieler, L.H., and Walther, B. (2009).
Prevalence of methicillin-resistant Staphylococcus pseudointermedius isolated from
clinical samples of companion animals and equidaes. Veterinary Microbiology, 136,
197-201. doi:10.1016/j.vetmic.2008.10.023
Show, A.C., Joshi, S., Greenwood, H., Panda, A., and Lord, J.M. (2012). Aging of the innate
immune system. Current Opinion in Immunology, 22, 507-513.
doi:10.1016/j.coi.2010.05.003
Sievert, D.M., Ricks, P., Edwards, J.R., Schneider, A., Patel, J., Srinivasan, A., … Fridkin, S.
(2013). Antimicrobial-resistant pathogens associated with healthcare-associated
infections: summary of data reported to the National Healthcare Safety Network at the
centers for disease control and prevention, 2009-2010. Infection Control and Hospital
Epidemiology, 34, 1-14. doi:10.1086/668770
Teira, R., Teira, A., Campo, A.B., and de Benito, I. (2013). Prevalence of nasopharyngeal
colonization by methicillin-resistent Staphylococcus aureus in a population of high
school students in Torrelavega (Spain). Enfermedades Infecciosas y Microbiología
Clínica, 31(5), 349. doi:10.1016/j.eimc.2012.10.006
Tong, S.Y.C., Davis, J.S., Eichemberger, E., Holland, T.L., and Fowler, V.C. Jr. (2015).
Staphylococcus aureus infections: epidemiology, pathophysiology, clinical
manifestations, and management. Clinical Microbiology Reviews, 28, 603-661.
doi:10.1128/CMR.00134-14
Van Bijnen, E.M.E., Paget, J., de Lange-de Klerk, E.S.M., den Heijer, C.D.J., Versporten, A.,
Stobberingh, E.E.,… Schellevis, F.G. (2015). Antibiotic exposure and other risk factors
for antimicrobial resistance in nasal commensal Staphylococcus aureus: an ecological
study in 8 european countries. PLoS ONE, 10(8), e0135093.
doi:10.1371/journal.pone.0135094
Vindel, A., Trincado, P., Cuevas, O., Ballesteros, C, Bouza, E., and Cercenado, E. (2014).
Molecular epidemiology of community-associated methicillin resistant Staphylococcus
aureus in Spain: 2004-2012. Journal of Antimicrobial Chemotherapy, 69, 2913-2919.
doi:10.1093/jac/dku232
Wang, H.K., Huang, C.Y., Chen, C.J., and Huang, Y.C. (2017). Nasal Staphylococcus aureus
carriage among college student athletes in northern Taiwan. Journal of Microbiology,
Immunology and Infection, 50, 537-540. doi:10.1016/j.jmii.2016.11.005
Weidenmaier, C., Goerke, C., and Wolz, C. (2012). Staphylococcus aureus determinants for nasal
colonization. Trends in Microbiology, 20, 243-250. doi:10.1016/j.tim.2012.03.004
Wertheim, H.F., Vos, M.C., Ott, A., van Belkum, A., Voss, A., Kluytmans, J.A.,… Verbrugh,
H.A. (2004). Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in
nasal carriers versus non-carriers. Lancet, 364, 703.705. doi:10.1016/S0140-
6736(04)16897-9