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International Journal of Microbiology
Volume 2017, Article ID 4287547, 11 pages
https://doi.org/10.1155/2017/4287547
Research Article

Staphylococcus saprophyticus Recovered from Humans, Food, and Recreational Waters in Rio de Janeiro, Brazil

1Laboratório de Investigação em Microbiologia Médica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil
2School of Public Health, University of California, Berkeley, Berkeley, CA, USA
3Instituto Biomédico, Universidade Federal Fluminense, Niterói, RJ, Brazil

Correspondence should be addressed to Beatriz Meurer Moreira; rb.jrfu.orcim@reruemb

Received 23 February 2017; Accepted 19 April 2017; Published 24 May 2017

Academic Editor: Todd R. Callaway

Copyright © 2017 Viviane Santos de Sousa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Eriksson, C. G. Giske, and A. Ternhag, “The relative importance of Staphylococcus saprophyticus as a urinary tract pathogen: distribution of bacteria among urinary samples analysed during 1 year at a major Swedish laboratory,” Acta Pathologica, Microbiologica, et Immunologica Scandinavica, vol. 121, no. 1, pp. 72–78, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. J. C. Soares, M. R. Marques, F. K. Tavaria, J. O. Pereira, F. X. Malcata, and M. M. Pintado, “Biodiversity and characterization of Staphylococcus species isolated from a small manufacturing dairy plant in Portugal,” International Journal of Food Microbiology, vol. 146, no. 2, pp. 123–129, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. E. Coton, M.-H. Desmonts, S. Leroy et al., “Biodiversity of coagulase-negative Staphylococci in french cheeses, dry fermented sausages, processing environments and clinical samples,” International Journal of Food Microbiology, vol. 137, no. 2-3, pp. 221–229, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. A. M. M. Abd-Elall, M. E. M. Mohamed, and M. A. I. Awadallah, “Potential airborne microbial hazards for workers on dairy and beef cattle farms in Egypt,” Veterinaria Italiana, vol. 45, no. 2, pp. 275–285, 2009. View at Google Scholar
  5. S. Leroy, P. Giammarinaro, J.-P. Chacornac, I. Lebert, and R. Talon, “Biodiversity of indigenous staphylococci of naturally fermented dry sausages and manufacturing environments of small-scale processing units,” Food Microbiology, vol. 27, no. 2, pp. 294–301, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. V. L. M. Rall, J. M. Sforcin, M. F. R. de Deus et al., “Polymerase chain reaction detection of enterotoxins genes in coagulase-negative staphylococci isolated from Brazilian minas cheese,” Foodborne Pathogens and Disease, vol. 7, no. 9, pp. 1121–1123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. A. P. Basso, P. D. Martins, G. Nachtigall, S. van der Sand, T. M. de Moura, and A. P. G. Frazzon, “Antibiotic resistance and enterotoxin genes in Staphylococcus sp. Isolates from polluted water in southern Brazil,” Anais da Academia Brasileira de Ciencias, vol. 86, no. 4, pp. 1813–1820, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Harakeh, H. Yassine, S. Hajjar, and M. El-Fadel, “Isolates of Staphylococcus aureus and saprophyticus resistant to antimicrobials isolated from the Lebanese aquatic environment,” Marine Pollution Bulletin, vol. 52, no. 8, pp. 912–919, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Sergelidis, A. Abrahim, T. Papadopoulos et al., “Isolation of methicillin-resistant Staphylococcus spp. from ready-to-eat fish products,” Letters in Applied Microbiology, vol. 59, no. 5, pp. 500–506, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. B.-S. Kim, C.-T. Kim, B. H. Park et al., “Draft genome sequence of Staphylococcus saprophyticus subsp. saprophyticus M1-1, isolated from the gills of a Korean rockfish, sebastes schlegeli hilgendorf, after high hydrostatic pressure processing,” Journal of Bacteriology, vol. 194, no. 16, pp. 4441-4442, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. V. S. de Sousa, R. F. Rabello, R. C. D. S. Dias et al., “Time-based distribution of Staphylococcus saprophyticus pulsed field gel-electrophoresis clusters in community-acquired urinary tract infections,” Memorias do Instituto Oswaldo Cruz, vol. 108, no. 1, pp. 73–76, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Sousa, N. Silva, G. Igrejas et al., “Antimicrobial resistance determinants in Staphylococcus spp. recovered from birds of prey in Portugal,” Veterinary Microbiology, vol. 171, no. 3-4, pp. 436–440, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. M. A. Fernández-Fuentes, H. Abriouel, E. Ortega Morente, R. Pérez Pulido, and A. Gálvez, “Genetic determinants of antimicrobial resistance in Gram positive bacteria from organic foods,” International Journal of Food Microbiology, vol. 172, pp. 49–56, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Le Bouter, R. Leclercq, and V. Cattoir, “Molecular basis of resistance to macrolides, lincosamides and streptogramins in Staphylococcus saprophyticus clinical isolates,” International Journal of Antimicrobial Agents, vol. 37, no. 2, pp. 118–123, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. O. C. Sampimon, T. J. G. M. Lam, D. J. Mevius, Y. H. Schukken, and R. N. Zadoks, “Antimicrobial susceptibility of coagulase-negative staphylococci isolated from bovine milk samples,” Veterinary Microbiology, vol. 150, no. 1-2, pp. 173–179, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Söderquist and C. Berglund, “Methicillin-resistant Staphylococcus saprophyticus in Sweden carries various types of staphylococcal cassette chromosome mec (SCCmec),” Clinical Microbiology and Infection, vol. 15, no. 12, pp. 1176–1178, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. D. T. Dubin, J. E. Fitzgibbon, M. D. Nahvi, and J. F. John, “Topoisomerase sequences of coagulase-negative staphylococcal isolates resistant to ciprofloxacin or trovafloxacin,” Antimicrobial Agents and Chemotherapy, vol. 43, no. 7, pp. 1631–1637, 1999. View at Google Scholar · View at Scopus
  18. P. A. Jordan, A. Iravani, G. A. Richard, and H. Baer, “Urinary tract infection caused by Staphylococcus saprophyticus,” Journal of Infectious Diseases, vol. 142, no. 4, pp. 510–515, 1980. View at Publisher · View at Google Scholar · View at Scopus
  19. F.-J. Schmitz, A. C. Fluit, M. Gondolf et al., “The prevalence of aminoglycoside resistance and corresponding resistance genes in clinical isolates of staphylococci from 19 European hospitals,” Journal of Antimicrobial Chemotherapy, vol. 43, no. 2, pp. 253–259, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. M. C. P. Nguyen, P.-L. Woerther, M. Bouvet, A. Andremont, R. Leclercq, and A. Canu, “Escherichia coli as reservoir for macrolide resistance genes,” Emerging Infectious Diseases, vol. 15, no. 10, pp. 1648–1650, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Lina, A. Quaglia, M.-E. Reverdy, R. Leclercq, F. Vandenesch, and J. Etienne, “Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci,” Antimicrobial Agents and Chemotherapy, vol. 43, no. 5, pp. 1062–1066, 1999. View at Google Scholar · View at Scopus
  22. F. Martineau, F. J. Picard, N. Lansac et al., “Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis,” Antimicrobial Agents and Chemotherapy, vol. 44, no. 2, pp. 231–238, 2000. View at Publisher · View at Google Scholar
  23. P. Lüthje and S. Schwarz, “Antimicrobial resistance of coagulase-negative staphylococci from bovine subclinical mastitis with particular reference to macrolide-lincosamide resistance phenotypes and genotypes,” Journal of Antimicrobial Chemotherapy, vol. 57, no. 5, pp. 966–969, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Santagati, F. Iannelli, M. R. Oggioni, S. Stefani, and G. Pozzi, “Characterization of a genetic element carrying the macrolide efflux gene mef(A) in Streptococcus pneumoniae,” Antimicrobial Agents and Chemotherapy, vol. 44, no. 9, pp. 2585–2587, 2000. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Zhang, J.-A. McClure, S. Elsayed, T. Louie, and J. M. Conly, “Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus,” Journal of Clinical Microbiology, vol. 43, no. 10, pp. 5026–5033, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. M. A. Argudin, B. A. Tenhagen, A. Fetsch et al., “Virulence and resistance determinants of german Staphylococcus aureus ST398 isolates from nonhuman sources,” Applied and Environmental Microbiology, vol. 77, no. 9, pp. 3052–3060, 2011. View at Publisher · View at Google Scholar
  27. G. E. Dale, H. Langen, M. G. P. Page, R. L. Then, and D. Stuber, “Cloning and characterization of a novel, plasmid-encoded trimethoprim- resistant dihydrofolate reductase from Staphylococcus haemolyticus MUR313,” Antimicrobial Agents and Chemotherapy, vol. 39, no. 9, pp. 1920–1924, 1995. View at Publisher · View at Google Scholar · View at Scopus
  28. S. R. Stengren and M. J. Starzyk, “A modified medium for the recovery of Staphylococcus from water,” Microbios, vol. 41, no. 165-166, pp. 191–203, 1984. View at Google Scholar · View at Scopus
  29. Y. Salfinger and M. L. Tortorello, Compendium of Methods for the Microbiological Examination of Foods, American Public Health Association, Washington, DC, USA, 2001. View at Publisher · View at Google Scholar
  30. L. F. Montezzi, E. H. Campana, L. L. Corrêa et al., “Occurrence of carbapenemase-producing bacteria in coastal recreational waters,” International Journal of Antimicrobial Agents, vol. 45, no. 2, pp. 174–177, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. T. L. Bannerman and S. J. Peacock, “Staphylococcus Micrococcus, and other catalase- positive cocci,” in Manual of Clinical Microbiology, P. R. Murray, E. L. Baron, J. H. Jorgensen, M. L. Landry, and M. A. Pfaller, Eds., pp. 390–401, Washington, DC, USA, 2007. View at Google Scholar
  32. T.-F. Lee, H. Lee, C.-M. Chen et al., “Comparison of the accuracy of matrix-assisted laser desorption ionization-time of flight mass spectrometry with that of other commercial identification systems for identifying Saphylococcus saprophyticus in urine,” Journal of Clinical Microbiology, vol. 51, no. 5, pp. 1563–1566, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. CLSI, Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically: Approved Standard, Clinical and Laboratory Standards Institute, Pa, USA, 9th, (M07-A9) edition, 2012.
  34. CLSI., Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement, Clinical and Laboratory Standards Institute, Pa, USA, 2015.
  35. M. Yamada, J. Yoshida, S. Hatou, T. Yoshida, and Y. Minagawa, “Mutations in the quinolone resistance determining region in Staphylococcus epidermidis recovered from conjunctiva and their association with susceptibility to various fluoroquinolones,” British Journal of Ophthalmology, vol. 92, no. 6, pp. 848–851, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. L. J. V. Piddock, “Mechanisms of fluoroquinolone resistance: an update 1994–1998,” Drugs, vol. 58, no. 2, pp. 11–18, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. R. F. Rabello, C. R. V. M. Souza, R. S. Duarte, R. M. M. Lopes, L. M. Teixeira, and A. C. D. Castro, “Characterization of Staphylococcus aureus isolates recovered from bovine mastitis in Rio de Janeiro, Brazil,” Journal of Dairy Science, vol. 88, no. 9, pp. 3211–3219, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. K. M. Sullivan, A. Dean, and M. M. Soe, “OpenEpi: a web-based epidemiologic and statistical calculator for public health,” Public Health Reports, vol. 124, no. 3, pp. 471–474, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Hedman, O. Ringertz, K. Olsson, and R. Wollin, “Plasmid-identified Staphylococcus saprophyticus isolated from the rectum of patients with urinary tract infections,” Scandinavian Journal of Infectious Diseases, vol. 23, no. 5, pp. 569–572, 1991. View at Publisher · View at Google Scholar · View at Scopus
  40. M. E. Rupp, D. E. Soper, and G. L. Archer, “Colonization of the female genital tract with Staphylococcus saprophyticus,” Journal of Clinical Microbiology, vol. 30, no. 11, pp. 2975–2979, 1992. View at Google Scholar
  41. T. Spanu, E. De Carolis, B. Fiori et al., “Evaluation of matrix-assisted laser desorption ionization-time-of-flight mass spectrometry in comparison to rpoB gene sequencing for species identification of bloodstream infection staphylococcal isolates,” Clinical Microbiology and Infection, vol. 17, no. 1, pp. 44–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. H. C. Lichstein and M. H. Soule, “Studies of the effect of sodium azide on microbic growth and respiration,” Journal of Bacteriology, vol. 47, no. 3, pp. 221–230, 1944. View at Google Scholar
  43. K. Gupta et al., “International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the infectious diseases society of america and the european society for microbiology and infectious diseases,” Clinical Infectious Diseases, vol. 52, no. 5, pp. e103–e120, 2011. View at Google Scholar
  44. C. Strauss, Y. Hu, A. Coates, and V. Perreten, “A novel erm(44) gene variant from a human Staphylococcus saprophyticus confers resistance to macrolides, lincosamides but not streptogramins,” Antimicrobial Agents and Chemotherapy, vol. 61, no. 1, Article ID e01655-16, 2016. View at Publisher · View at Google Scholar
  45. M. Higashide, M. Kuroda, S. Ohkawa, and T. Ohta, “Evaluation of a cefoxitin disk diffusion test for the detection of mecA-positive methicillin-resistant Staphylococcus saprophyticus,” International Journal of Antimicrobial Agents, vol. 27, no. 6, pp. 500–504, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Matuszkiewicz-Rowińska, J. Małyszko, and M. Wieliczko, “Urinary tract infections in pregnancy: old and new unresolved diagnostic and therapeutic problems,” Archives of Medical Science, vol. 11, no. 1, pp. 67–77, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Lee, P. Bozzo, A. Einarson, and G. Koren, “Urinary tract infections in pregnancy,” Canadian Family Physician, vol. 54, no. 6, pp. 853-854, 2008. View at Google Scholar · View at Scopus
  48. F. Chereau, P. Herindrainy, B. Garin et al., “ESBL- and NDM-1-producing Enterobacteriaceae colonization among pregnant women in the community in a low income country: a potential reservoir for transmission of multi-resistant Enterobacteriaceae to neonates,” Antimicrobial Agents and Chemotherapy, vol. 59, no. 6, pp. 3652–3655, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. L. A. Denkel, F. Schwab, A. Kola et al., “The mother as most important risk factor for colonization of very low birth weight (VLBW) infants with extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-E),” Journal of Antimicrobial Chemotherapy, vol. 69, no. 8, Article ID dku097, pp. 2230–2237, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Pathak, S. P. Chandran, K. Mahadik, R. Macaden, and C. S. Lundborg, “Frequency and factors associated with carriage of multi-drug resistant commensal Escherichia coli among women attending antenatal clinics in Central India,” BMC Infectious Diseases, vol. 13, no. 1, article 199, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Widerström, J. Wiström, S. Ferry, C. Karlsson, and T. Monsen, “Molecular epidemiology of Staphylococcus saprophyticus isolated from women with uncomplicated community-acquired urinary tract infection,” Journal of Clinical Microbiology, vol. 45, no. 5, pp. 1561–1564, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. P. Hedman and O. Ringertz, “Urinary tract infections caused by Staphylococcus saprophyticus. a matched case control study,” Journal of Infection, vol. 23, no. 2, pp. 145–153, 1991. View at Publisher · View at Google Scholar · View at Scopus
  53. N. H. Khan, M. Ahsan, W. D. Taylor, and K. Kogure, “Culturability and survival of marine, freshwater and clinical Pseudomonas aeruginosa,” Microbes and Environments, vol. 25, no. 4, pp. 266–274, 2010. View at Publisher · View at Google Scholar · View at Scopus