This study focused on the presence of antibiotic-resistant bacteria in a metro system as an example of a public transportation system. The molecular characteristics of Staphylococcus were investigated to discern which strains were isolated from metro stations in Shanghai. These were compared with strains isolated from hospital treatment rooms and parks. Airborne Staphylococcus samples in the metro were resistant to an average of 2.64 antibiotic types, and 58.0% of the strain samples were resistant to at least three antibiotics; this was a significantly higher rate than strains from the park, but was lower than those from hospitals. The presence of two antibiotic resistance genes of Staphylococcus strains, mecA (28.0%) and qac (40.0%), were also found at significantly higher levels in metro samples than park samples, but did not differ significantly from hospital samples. Furthermore, 22.0% of the metro Staphylococcus samples were found to be biofilm-positive. The high rate of antibiotic resistance found in Staphylococcus samples collected from metro stations, and the discovery of antibiotic-resistant genes, indicate that the closed indoor environment and crowded passengers may accelerate the spread of antibiotic resistant strains. More attention should be paid to the inspection and control of antibiotic resistant strains in public transportation systems.
References
[1]
Baba, T.; Takeuchi, F.; Kuroda, M.; Yuzawa, H.; Aoki, K.; Oguchi, A.; Nagai, Y.; Iwama, N.; Asano, K.; Naimi, T.; et al. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 2002, 359, 1819–1827, doi:10.1016/S0140-6736(02)08713-5.
[2]
Sobhy, N.; Aly, F.; Abd El Kader, O.; Ghazal, A.; Elbaradei, A. Community-acquired methicillin-resistant Staphylococcus aureus from skin and soft tissue infections (in a sample of Egyptian population): Analysis of mec gene and staphylococcal cassette chromosome. Braz. J. Infect. Dis. 2012, 16, 426–431, doi:10.1016/j.bjid.2012.08.004.
[3]
Nobile, C.; Costantino, R.; Bianco, A.; Pileggi, C.; Pavia, M. Prevalence and pattern of antibiotic resistance of Campylobacter spp. in poultry meat in Southern Italy. Food Control 2013, 32, 715–718, doi:10.1016/j.foodcont.2013.02.011.
[4]
Reynolds, K.A.; Watt, P.M.; Boone, S.A.; Gerba, C.P. Occurrence of bacteria and biochemical markers on public surfaces. Int. J. Environ. Health Res. 2005, 15, 225–234, doi:10.1080/09603120500115298.
[5]
Dybwad, M.; Granum, P.E.; Bruheim, P.; Blatny, J.M. Characterization of airborne bacteria at an underground subway station. Appl. Environ. Microbiol. 2012, 78, 1917–1929, doi:10.1128/AEM.07212-11.
[6]
Gilleberg, S.B.; Faull, J.L.; Graeme-Cook, K.A. A preliminary survey of aerial biocontaminants at six London underground stations. Int. Biodeterior. Biodegrad. 1998, 41, 149–152, doi:10.1016/S0964-8305(98)00005-5.
[7]
Awad, A.H.A. Environmental study in subway metro stations in Cairo, Egypt. J. Occup. Health 2002, 44, 112–118, doi:10.1539/joh.44.112.
[8]
Hwang, S.H.; Yoon, C.S.; Ryu, K.N.; Paik, S.Y.; Cho, J.H. Assessment of airborne environmental bacteria and related factors in 25 underground railway stations in Seoul, Korea. Atmos. Environ. 2010, 44, 1658–1662, doi:10.1016/j.atmosenv.2010.01.047.
[9]
Kawasaki, T.; Kyotani, T.; Ushiogi, T.; Izumi, Y.; Lee, H.; Hayakawa, T. Distribution and identification of airborne fungi in railway stations in Tokyo, Japan. J. Occup. Health 2010, 52, 186–193, doi:10.1539/joh.O9022.
[10]
Dong, S.; Yao, M. Exposure assessment in Beijing, China: Biological agents, ultrafine particles, and lead. Environ. Monit. Assess. 2010, 170, 331–343, doi:10.1007/s10661-009-1236-7.
[11]
Yeh, P.; Simon, D.; Millar, J.; Alexander, F.; Franklin, D. A diversity of antibiotic-resistant Staphylococcus spp. in a public transportation system. Osong Public Health Res. Perspect. 2011, 2, 202–209, doi:10.1016/j.phrp.2011.11.047.
[12]
Mandell, G.L.; Bennett, J.E.; Dolin, R. Mandell, Dauglas and Bennett’s Principles and Practice of Infectious Diseases, 5th ed. ed.; Churchill Livingstone Inc: Philadelphia, PA, USA, 2000; p. 2049.
[13]
Schreckenberger, P.C.; Ilendo, E.; Ristow, K.L. Incidence of constitutive and inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci in a community and a tertiary care hospital. J. Clin. Microbiol. 2004, 42, 2777–2779, doi:10.1128/JCM.42.6.2777-2779.2004.
[14]
O’Toole, G.; Kaplan, H.B.; Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 2000, 54, 49–79, doi:10.1146/annurev.micro.54.1.49.
[15]
Enright, M.C.; Robinson, D.A.; Randle, G.; Feil, E.J.; Grundmann, H.; Spratt, B.G. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc. Natl. Acad. Sci. USA 2002, 99, 7687–7692.
[16]
Koksal, F.; Yasar, H.; Samasti, M. Antibiotic resistance patterns of coagulase-negative Staphylococcus strains isolated from blood cultures of septicemic patients in Turkey. Microbiol. Res. 2009, 164, 404–410, doi:10.1016/j.micres.2007.03.004.
[17]
Poston, S.M.; Li Saw Hee, F.L. Genetic characterisation of resistance to metal ions in methicillin-resistant Staphylococcus aureus: Elimination of resistance to cadmium, mercury and tetracycline with loss of methicillin resistance. J. Med. Microbiol. 1991, 34, 193–201, doi:10.1099/00222615-34-4-193.
[18]
Mitchell, B.A.; Brown, M.H.; Skurray, R.A. QacA Multidrug Efflux Pump from Staphylococcus aureus: Comparative analysis of resistance to diamidines, biguanidines, and guanylhydrazones. Antimicrob. Agents Chemother. 1998, 42, 475–477, doi:10.1093/jac/42.4.475.
[19]
Ministry of Health Law and Oversight Division. Disinfection Technical Specifications; Ministry of Health: Beijing, China, 2002.
[20]
Onni, T.; Sanna, G.; Cubeddu, G.P.; Marogna, G.; Lollai, S.; Leori, G.; Tola, S. Identification of coagulase-negative staphylococci isolated from ovine milk samples by PCR-RFLP of 16S rRNA and gap genes. Vet. Microbiol. 2010, 144, 347–352, doi:10.1016/j.vetmic.2010.01.016.
[21]
Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731–2739, doi:10.1093/molbev/msr121.
Li, M.; Wang, X.; Gao, Q.; Lu, Y. Molecular characterization of Staphylococcus epidermidis strains isolated from a teaching hospital in Shanghai, China. J. Med. Microbiol. 2009, 58, 456–461, doi:10.1099/jmm.0.007567-0.
[24]
Wang, L.; Li, M.; Dong, D.; Bach, T.H.; Sturdevant, D.E.; Vuong, C.; Otto, M.; Gao, Q. SarZ is a key regulator of biofilm formation and virulence in Staphylococcus epidermidis. J. Infect. Dis. 2008, 197, 1254–1262, doi:10.1086/586714.
[25]
Koskela, A.; Nilsdotter-Augustinsson, ？.; Persson, L.; S？derquist, B. Prevalence of the ica operon and insertion sequence IS256 among Staphylococcus epidermidis prosthetic joint infection isolates. Eur. J. Clin. Microbiol. Infect. Dis. 2009, 28, 655–660, doi:10.1007/s10096-008-0664-6.
[26]
The World Health Report; World Health Organization: Geneva, Switzerland, 1996.
[27]
Cosgrove, S.E.; Sakoulas, G.; Perencevich, E.N.; Schwaber, M.J.; Karchmer, A.W.; Carmeli, Y. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: A meta-analysis. Clin. Infect. Dis. 2003, 36, 53–59, doi:10.1086/345476.
[28]
Harbarth, S.; Rutschmann, O.; Sudre, P.; Pittet, D. Impact of methicillin resistance on the outcome of patients with bacteremia caused by Staphylococcus aureus. Arch. Intern. Med. 1998, 158, 182–189, doi:10.1001/archinte.158.2.182.
[29]
Gillespie, B.E.; Headrick, S.I.; Boonyayatra, S.; Oliver, S.P. Prevalence and persistence of coagulase-negative Staphylococcus species in three dairy research herds. Vet. Microbiol. 2009, 134, 65–72, doi:10.1016/j.vetmic.2008.09.007.
[30]
Lorenz, M.G.; Wackernagel, W. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 1994, 58, 563–602.
[31]
Zhu, B. Degradation of plasmid and plant DNA in water microcosms monitored by natural transformation and real-time polymerase chain reaction (PCR). Water Res. 2006, 40, 3231–3238, doi:10.1016/j.watres.2006.06.040.
[32]
Hyder, S.L.; Streitfeld, M.M. Transfer of erythromycin resistance from clinically isolated lysogenic strains of Streptococcus pyogenes via their endogenous phage. J. Infect. Dis. 1978, 138, 281–286, doi:10.1093/infdis/138.3.281.
[33]
Blahova, J.; Hupkova, M.; Babalova, M.; Krcmery, V.; Schafer, V. Transduction of resistance to imipenem, aztreonam and ceftazidime in nosocomial strains of Pseudomonas aeruginosa by wild-type phages. Acta Virol. 1993, 37, 429–436.
[34]
Banks, D.J.; Porcella, S.F.; Barbian, K.D.; Beres, S.B.; Philips, L.E.; Voyich, J.M.; DeLeo, F.R.; Martin, J.M.; Somerville, G.A.; Musser, J.M. Progress toward characterization of the group A streptococcus metagenome: Complete genome sequence of a macrolide-resistant serotype M6 strain. J. Infect. Dis. 2004, 190, 727–738, doi:10.1086/422697.
[35]
Kuenne, C.; Voget, S.; Pischimarov, J.; Oehm, S.; Goesmann, A.; Daniel, R.; Hain, T.; Chakraborty, T. Comparative analysis of plasmids in the genus Listeria. PLoS ONE 2010, 5, e12511, doi:10.1371/journal.pone.0012511.
[36]
Luo, M.; Fei, Y.E.; Wang, D.M.; He, J.L.; Zhong, H.Y. Analysis of coagulase-negative Staphylococcus from sputum. J. Modern Clin. Med. 2010, 5, 83–84.
[37]
Cosgrove, S.E.; Sakoulas, G.; Perencevich, E.N.; Schwaber, M.J.; Karchmer, A.W.; Carmeli, Y. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: A meta-analysis. Clin. Infect. Dis. 2003, 36, 53–59, doi:10.1086/345476.
[38]
Harbarth, S.; Rutschmann, O.; Sudre, P.; Pittet, D. Impact of methicillin resistance on the outcome of patients with bacteremia caused by Staphylococcus aureus. Arch. Intern. Med. 1998, 158, 182–189, doi:10.1001/archinte.158.2.182.
[39]
Hisata, K.; Ito, T.; Matsunaga, N.; Komatsu, M.; Jin, J.; Li, S.; Watanabe, S.; Shimizu, T.; Hiramatsu, K. Dissemination of multiple MRSA clones among community-associated methicillin-resistant Staphylococcus aureus infections from Japanese children with impetigo. J. Infect. Chemother. 2011, 17, 609–621, doi:10.1007/s10156-011-0223-4.
[40]
Barbier, F.; Ruppé, E.; Hernandez, D.; Lebeaux, D.; Francois, P.; Felix, B.; Desprez, A.; Maiga, A.; Woerther, P.L.; Gaillard, K.; et al. Methicillin-resistant coagulase-negative staphylococci in the community: High homology of SCCmec IVa between Staphylococcus epidermidis and major clones of methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 2010, 202, 270–281.
[41]
Schnellmann, C.; Gerber, V.; Rossano, A.; Jaquier, V.; Panchaud, Y.; Doherr, M.G.; Thomann, A.; Straub, R.; Perreten, V. Presence of new MecA and mph(C) variants conferring antibiotic resistance in Staphylococcus spp. isolated from the skin of horses before and after clinic admission. J. Clin. Microbiol. 2006, 44, 4444–4454, doi:10.1128/JCM.00868-06.
[42]
Soge, O.O.; Meschke, J.S.; No, D.B.; Roberts, M.C. Characterization of methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative Staphylococcus spp. Isolated from US West Coast public marine beaches. J. Antimicrob. Chemother. 2009, 64, 1148–1155, doi:10.1093/jac/dkp368.
[43]
Wei, W.P. Distribution and drug-resistance of 408 strains of coagulase negative Staphylococcus. China Prac. Med. 2010, 5, 67–69.
[44]
Heir, E.; Sundheim, G.; Holck, A.L. The Staphylococcus qacH gene product: A new member of the SMR family encoding multidrug resistance. FEMS Microbiol. Lett. 1998, 163, 49–56, doi:10.1111/j.1574-6968.1998.tb13025.x.
[45]
Luthje, P.; von Kockritz-Blickwede, M.; Schwarz, S. Identification and characterization of nine novel types of small staphylococcal plasmids carrying the lincosamide. J. Antimicrob. Chemother. 2007, 59, 600–606, doi:10.1093/jac/dkm008.
[46]
Bjorland, J.; Steinum, T.; Sunde, M.; Waage, S.; Heir, E. Novel plasmid-borne gene qacJ mediates resistance to quaternary ammonium compounds in equine Staphylococcus aureus, Staphylococcus simulans, and Staphylococcus intermedius. Antimicrob. Agents Chemother. 2003, 47, 3046–3052, doi:10.1128/AAC.47.10.3046-3052.2003.
[47]
O’Toole, G.; Kaplan, H.B.; Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 2000, 54, 49–79, doi:10.1146/annurev.micro.54.1.49.
