This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ahmed, A. M.
Right arrow Articles by Shimamoto, T.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ahmed, A. M.
Right arrow Articles by Shimamoto, T.
Agricola
Right arrow Articles by Ahmed, A. M.
Right arrow Articles by Shimamoto, T.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, October 2007, p. 6686-6690, Vol. 73, No. 20
0099-2240/07/$08.00+0     doi:10.1128/AEM.01054-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Zoo Animals as Reservoirs of Gram-Negative Bacteria Harboring Integrons and Antimicrobial Resistance Genes{triangledown}

Ashraf M. Ahmed,1,3 Yusuke Motoi,1 Maiko Sato,1 Akito Maruyama,1 Hitoshi Watanabe,2 Yukio Fukumoto,2 and Tadashi Shimamoto1*

Laboratory of Food Microbiology and Hygiene, Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima 739-8528, Japan,1 Hiroshima City Asa Zoological Park, Asa-cho Asakita-ku, Hiroshima 731-3355, Japan,2 Department of Microbiology, Faculty of Veterinary Medicine, Kafr El-Sheikh University, Kafr El-Sheikh 33516, Egypt3

Received 11 May 2007/ Accepted 14 August 2007


arrow
ABSTRACT
 
A total of 232 isolates of gram-negative bacteria were recovered from mammals, reptiles, and birds housed at Asa Zoological Park, Hiroshima prefecture, Japan. Forty-nine isolates (21.1%) showed multidrug resistance phenotypes and harbored at least one antimicrobial resistance gene. PCR and DNA sequencing identified class 1 and class 2 integrons and many ß-lactamase-encoding genes, in addition to a novel AmpC ß-lactamase gene, blaCMY-26. Furthermore, the plasmid-mediated quinolone resistance genes qnr and aac(6')-Ib-cr were also identified.


arrow
INTRODUCTION
 
Problems associated with the development and spread of antibiotic resistance in clinical practice have been increasing since the early 1960s and are currently viewed as a major threat to the public health on a global level (15). Animals, particularly wild animals, are believed to be the source of >70% of all emerging infections (13). A recent report identified more than 25 human infectious disease outbreaks over a 10-year period (1990 to 2000) as being associated with visits to animal exhibits (2). Of particular concern is the potential transmission of multidrug-resistant zoonotic pathogens from zoo animals to humans. As little is known about antimicrobial-resistant bacteria in zoo animals, this study was conducted to monitor the incidence and prevalence of antimicrobial resistance genes in gram-negative bacteria isolated from zoo animals in Japan.

A total of 103 swabs (68 fecal, 33 water, and 2 nasal swabs) were randomly taken from different mammals, reptiles, birds, and water sources between June and September 2006 at Asa Zoological Park, Hiroshima prefecture, Japan. A total of 232 gram-negative bacteria were isolated, and the biochemical identification showed that the most prevalent species was Escherichia coli (122 isolates; 52.6%), followed by Klebsiella pneumoniae (17 isolates; 7.3%), Proteus mirabilis (16 isolates; 6.9%), Enterobacter aerogenes (14 isolates; 6.0%), Klebsiella oxytoca (13 isolates; 5.6%), Pseudomonas aeruginosa (12 isolates; 5.2%), Enterobacter cloacae (11 isolates; 4.7%), Proteus vulgaris (5 isolates; 2.2%), Citrobacter koseri (5 isolates; 2.2%), Citrobacter freundii (4 isolates; 2.2%), Morganella morganii (4 isolates; 1.7%), Salmonella spp. (3 isolates; 1.3%), Serratia marcescens (2 isolates; 0.9%), and a single isolate (0.43%) of Acinetobacter baumannii, Aeromonas spp., Pseudomonas fluorescens, and Edwardsiella tarda.

The antimicrobial sensitivity phenotypes of recovered bacteria were determined by using a disk diffusion assay according to the standards and interpretive criteria described by CLSI (5). The results showed that 49 isolates (21.1%) showed resistance phenotypes to two or more antimicrobial agents. The most commonly reported resistance phenotypes were against ampicillin, cephalothin, streptomycin, trimethoprim-sulfamethoxazole, kanamycin, tetracycline, nalidixic acid, and ciprofloxacin. Similar resistance phenotypes have been recorded previously for strains of E. coli isolated from wild animals in Portugal, from free-living Canada geese in Georgia and North Carolina, and from black-headed gulls in the Czech Republic (6-8). Interestingly, many isolates showed resistance phenotypes to extended-spectrum ß-lactam antibiotics, such as cefotaxime, ceftazidime, cefpodoxime, ceftriaxone and aztreonam, which are widely used for the treatment of serious infections in hospitals (3).

Integrons play a major role in the spread of antibiotic resistance genes in gram-negative bacteria (28). In this study, primers 5'-CS and 3'-CS, which amplify the region between the 5' conserved segment and 3' conserved segment of class 1 integrons, were used as previously described (Table 1) (14). PCR screening detected class 1 integrons in 16 bacterial isolates (6.9%); 11 E. coli isolates, 2 P. vulgaris isolates, and 1 isolate of E. cloacae, M. morganii, and P. mirabilis (Table 2). DNA sequencing results for the inserted gene cassettes identified seven profiles of class 1 integrons (Table 2). The identified antimicrobial resistance genes were dfrA1, dfrA5, dfrA12, dfrA15, and dfrA17, dihydrofolate reductase types which confer resistance to trimethoprim, and aadA1, aadA2 and aadA5, aminoglycoside adenyltransferase types which confer resistance to streptomycin and spectinomycin. The resistance phenotypes were expressed for most of these genes (Table 2). It was of interest that class 1 integrons harboring aadA1 have been previously identified for E. coli isolated from free-living Canada geese in Georgia and North Carolina and black-headed gulls in the Czech Republic (6, 8), while another type of class 1 integron harboring aadA7 has been previously identified in an E. coli strain isolated from the Washington Zoo, Seattle, WA (17). On the other hand, for the detection of class 2 integrons, PCR was performed with the primer pair hep74 and hep51, specific to the conserved regions of class 2 integrons, as described previously (Table 1) (31). Class 2 integrons were detected in four isolates (1.7%), including three E. coli isolates and one P. mirabilis isolate (Table 2). DNA sequencing results for the inserted gene cassettes within class 2 integrons identified the three classic resistance genes dfrA1, sat2, and aadA1, which are usually associated with transposon Tn7 (11). To the best of our knowledge, this is the first report for class 2 integrons from zoo animals.


View this table:
[in this window]
[in a new window]

  		TABLE 1. Primers used in this study


View this table:
[in this window]
[in a new window]

  		TABLE 2. Resistance phenotype and prevalence of integrons and resistance genes in gram-negative bacteria

Resistance to ß-lactam antibiotics in gram-negative bacteria is mediated primarily by ß-lactamases (3, 23). The bacterial isolates were tested for TEM, SHV, CTX-M, OXA, and CMY ß-lactamase-encoding genes by PCR using universal primers for the TEM, SHV, OXA, CTX-M and CMY families, as described previously (Table 1) (1, 33). Detection of the OXY ß-lactamase-encoding gene in K. oxytoca was carried out as described previously (10). PCR and DNA sequencing screenings detected blaTEM-1, a narrow-spectrum ß-lactamase gene which confers resistance against penicillins and narrow-spectrum cephalosporins, in 19 isolates (8.2%), which included 16 isolates of E. coli and 1 isolate of A. baumannii, P. mirabilis, and P. vulgaris (Table 2). All these isolates showed an ampicillin and cephalothin resistance phenotype (Table 2). TEM ß-lactamase has been previously detected in E. coli isolated from wild animals in Portugal (7) and from free-living Canada geese in Georgia and North Carolina and black-headed gulls in the Czech Republic (6, 8). blaOXY-2, another narrow-spectrum ß-lactamase, was identified in three strains of K. oxytoca. Interestingly, all three isolates are from reptiles (Japanese four-striped rat snake, Colombian rainbow boa, and giant salamander) (Table 2). blaOXY-2 is a K. oxytoca-linked ß-lactamase that confers resistance to narrow-spectrum cephalosporins and, to a lesser extent, to broad-spectrum cephalosporins, such as cefoperazone, and to monobactams, such as aztreonam (9). To the best of our knowledge, this is the first report of the blaOXY gene from zoo animals.

Recently, there has been a dramatic increase in the incidence and prevalence of extended-spectrum ß-lactamases (ESBLs) (3, 23). In this study, blaSHV-36, an ESBL-encoding gene, was identified in two isolates (0.9%), an E. coli isolate from birds and an E. cloacae isolate from a tortoise (Indotestudo elongata) (Table 2). blaSHV-36 was detected previously in a clinical isolate of Klebsiella spp. isolated from a fecal sample from a hospitalized patient in York, United Kingdom (19), while blaSHV-12 was identified previously from E. coli isolated from wild birds in Portugal (7). Furthermore, blaCTX-M-2, another ESBL-encoding gene, was identified in one E. coli isolate from the masked palm civet (Table 2). In Japan, blaCTX-M-2 was previously identified in ESBL-producing E. coli strains isolated from domestic animals (12, 29). It is worth noting that blaCTX-M-1 and blaCTX-M-14 have been previously isolated from wild animals in Portugal (7).

Furthermore, this study also identified a novel type of AmpC ß-lactamase-encoding gene named blaCMY-26, according to the previously assigned numbers of blaCMY. blaCMY-26 was identified in a single isolate of K. oxytoca from a jaybird. This K. oxytoca strain showed a typical AmpC ß-lactamase resistance phenotype, i.e., it was resistant to ampicillin, cephalothin, cefoxitin, cefotetan, ceftriaxone, and amoxicillin-clavulanic acid, in addition to other non-ß-lactam antibiotics, such as streptomycin and kanamycin (Table 2). The putative CMY-26 enzyme showed 98% amino acid identity to CMY-13 (accession number AY339625) (18).

In 1998, Martínez-Martínez et al. discovered plasmid-mediated quinolone resistance in a K. pneumoniae clinical strain isolate from Alabama (16). The gene responsible for quinolone resistance, qnr, encodes a protein of the pentapeptide repeat family, which has been shown to block the action of ciprofloxacin on purified DNA gyrase and topoisomerase IV (30). To date, three main types of qnr genes, qnrA, qnrB, and qnrS, have been identified (20, 25). In this study, different primers were used for the screening of the qnr-related genes qnrA, qnrB, and qnrS, as described previously (Table 1) (27). A multiplex PCR screening detected qnr genes in 10 (4.3%) of the tested isolates and, interestingly, 4 of them were from reptiles (Table 2). DNA sequencing results for the 10 PCR amplicons showed that 6 were qnrB and 4 were qnrS. The six qnrB genes were identified for E. coli, K. pneumoniae, K. oxytoca, C. freundii, P. mirabilis, and P. fluorescens (Table 2). Note that qnrB was previously identified for E. coli from K. pneumoniae in the United States (27) and Korea (21) and from C. freundii in Palestine (accession no. AB281054). However, to the best of our knowledge, this is the first report of qnrB in K. oxytoca, P. mirabilis, and P. fluorescens and is also the first report of the incidence of qnrB in Japan. The four qnrS genes were identified from three isolates of E. coli and one isolate of E. cloacae (Table 2). qnrS has been reported previously from human clinical isolates of E. coli in France and Scandinavia (4, 24) and has also been detected in clinical isolates of E. cloacae from France and Taiwan (24, 32).

More recently, a new mechanism of plasmid-associated quinolone resistance, involving the ciprofloxacin-modifying aminoglycoside acetyltransferase gene, aac(6')-Ib-cr, has been discovered (26). In this study, universal primers for detection of all types of aac(6')-Ib, including its variants, were used as described previously (22). PCR and DNA sequencing results identified aac(6')-Ib-cr, with the typical amino acid substitutions (Trp102Arg and Asp179Tyr) (26), in a single isolate of Aeromonas spp. (Table 2). The aac(6')-Ib-cr gene has been identified previously from E. coli, K. pneumoniae, and Enterobacter sp. isolates in the United States (22). To our knowledge, this is the first report for this gene in Japan.

In summary, the results of the current study highlight zoo animals as a potential reservoir of antimicrobial-resistant bacteria and clinically important resistance genes.


arrow
Nucleotide sequence accession number.
 
The nucleotide sequence of the new AmpC ß-lactamase gene, blaCMY-26, described in this study was deposited in GenBank under accession no. AB300358.


arrow
ACKNOWLEDGMENTS
 
A.M.A. is supported by a postdoctoral fellowship from the Japan Society for the Promotion of Science. This work was supported by a Grant-in-Aid for Scientific Research to T.S. from the Ministry of Education, Culture, Sports, Science and Technology of Japan.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Laboratory of Food Microbiology and Hygiene, Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima 739-8528, Japan. Phone and fax: 81 (82) 424 7897. E-mail: tadashis{at}hiroshima-u.ac.jp Back

{triangledown} Published ahead of print on 24 August 2007. Back


arrow
REFERENCES
 
    1
  1. Ahmed, A. M., K. Furuta, K. Shimomura, Y. Kasama, and T. Shimamoto. 2006. Genetic characterization of multidrug resistance in Shigella spp. from Japan. J. Med. Microbiol. 55:1685-1691.[Abstract/Free Full Text]
    2. 2
  2. Bender, J. B., and S. A. Shulman. 2004. Reports of zoonotic disease outbreaks associated with animal exhibits and availability of recommendations for preventing zoonotic disease transmission from animals to people in such settings. J. Am. Vet. Med. Assoc. 224:1105-1109.[CrossRef][Medline]
    3. 3
  3. Bradford, P. A. 2001. Extended-spectrum ß-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin. Microbiol. Rev. 14:933-951.[Abstract/Free Full Text]
    4. 4
  4. Cavaco, L. M., D. S. Hansen, A. Friis-Moller, F. M. Aarestrup, H. Hasman, and N. Frimodt-Moller. 2007. First detection of plasmid-mediated quinolone resistance (qnrA and qnrS) in Escherichia coli strains isolated from humans in Scandinavia. J. Antimicrob. Chemother. 59:804-805.[Free Full Text]
    5. 5
  5. Clinical and Laboratory Standards Institute. 2002. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Approved standard, 2nd ed. NCCLS document M31-A2. Clinical and Laboratory Standards Institute, Wayne, PA.
    6. 6
  6. Cole, D., D. J. V. Drum, D. E. Stallknecht, D. G. White, M. D. Lee, S. Ayers, M. Sobsey, and J. J. Maurer. 2005. Free-living Canada geese and antimicrobial resistance. Emerg. Infect. Dis. 11:935-938.[Medline]
    7. 7
  7. Costa, D., P. Poeta, Y. Saenz, L. Vinue, B. Rojo-Bezares, A. Jouini, M. Zarazaga, J. Rodrigues, and C. Torres. 2006. Detection of Escherichia coli harbouring extended-spectrum ß-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. J. Antimicrob. Chemother. 58:1311-1312.[Free Full Text]
    8. 8
  8. Dolejska, M., A. Cizek, and I. Literak. 2007. High prevalence of antimicrobial-resistant genes and integrons in Escherichia coli isolates from black-headed gulls in the Czech Republic. J. Appl. Microbiol. 103:11-19.[CrossRef][Medline]
    9. 9
  9. Farzaneh, S., J. Peduzzi, L. Sofer, A. Reynaud, M. Barthelemy, and R. Labia. 1997. Characterization and amino acid sequence of the OXY-2 group for ß-lactamase of pI 5.7 isolated from aztreonam-resistant Klebsiella oxytoca strain HB60. J. Antimicrob. Chemother. 40:789-795.[Abstract/Free Full Text]
    10. 10
  10. Fevre, C., M. Jbel, V. Passet, F. X. Weill, P. A. Grimont, and S. Brisse. 2005. Six groups of the OXY ß-lactamase evolved over millions of years in Klebsiella oxytoca. Antimicrob. Agents Chemother. 49:3453-3462.[Abstract/Free Full Text]
    11. 11
  11. Hansson, K., L. Sundström, A. Pelletier, and P. H. Roy. 2002. IntI2 integron integrase in Tn7. J. Bacteriol. 184:1712-1721.[Abstract/Free Full Text]
    12. 12
  12. Kojima, A., Y. Ishii, K. Ishihara, H. Esaki, T. Asai, C. Oda, Y. Tamura, T. Takahashi, and K. Yamaguchi. 2005. Extended-spectrum-ß-lactamase-producing Escherichia coli strains isolated from farm animals from 1999 to 2002: report from the Japanese Veterinary Antimicrobial Resistance Monitoring Program. Antimicrob. Agents Chemother. 49:3533-3537.[Abstract/Free Full Text]
    13. 13
  13. Kuiken, T., F. A. Leighton, R. A. Fouchier, J. W. LeDuc, J. S. Peiris, A. Schudel, K. Stohr, and A. D. Osterhaus. 2005. Public health: pathogen surveillance in animals. Science 309:1680-1681.[Abstract/Free Full Text]
    14. 14
  14. Lévesque, C., L. Piché, C. Larose, and P. H. Roy. 1995. PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob. Agents Chemother. 39:185-191.[Abstract]
    15. 15
  15. Levy, S. B., and B. Marshall. 2004. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10:S122-S129.[CrossRef][Medline]
    16. 16
  16. Martínez-Martínez, L., A. Pascual, and G. A. Jacoby. 1998. Quinolone resistance from a transferable plasmid. Lancet 351:797-799.[CrossRef][Medline]
    17. 17
  17. Mazel, D., B. Dychinco, V. A. Webb, and J. Davies. 2000. Antibiotic resistance in the ECOR collection: integrons and identification of a novel aad gene. Antimicrob. Agents Chemother. 44:1568-1574.[Abstract/Free Full Text]
    18. 18
  18. Miriagou, V., L. S. Tzouvelekis, L. Villa, E. Lebessi, A. C. Vatopoulos, A. Carattoli, and E. Tzelepi. 2004. CMY-13, a novel inducible cephalosporinase encoded by an Escherichia coli plasmid. Antimicrob. Agents Chemother. 48:3172-3174.[Abstract/Free Full Text]
    19. 19
  19. Munday, C. J., G. M. Whitehead, N. J. Todd, M. Campbell, and P. M. Hawkey. 2004. Predominance and genetic diversity of community- and hospital-acquired CTX-M extended-spectrum ß-lactamases in York, UK. J. Antimicrob. Chemother. 54:628-633.[Abstract/Free Full Text]
    20. 20
  20. Nordmann, P., and L. Poirel. 2005. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J. Antimicrob. Chemother. 56:463-469.[Abstract/Free Full Text]
    21. 21
  21. Pai, H., M.-R. Seo, and T. Y. Choi. 2007. Association of QnrB determinants and production of extended-spectrum ß-lactamases or plasmid-mediated AmpC ß-lactamases in clinical isolates of Klebsiella pneumoniae. Antimicrob. Agents Chemother. 51:366-368.[Abstract/Free Full Text]
    22. 22
  22. Park, C. H., A. Robicsek, G. A. Jacoby, D. Sahm, and D. C. Hooper. 2006. Prevalence in the United States of aac(6')-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob. Agents Chemother. 50:3953-3955.[Abstract/Free Full Text]
    23. 23
  23. Paterson, D. L., and R. A. Bonomo. 2005. Extended-spectrum ß-lactamases: a clinical update. Clin. Microbiol. Rev. 18:657-686.[Abstract/Free Full Text]
    24. 24
  24. Poirel, L., C. Leviandier, and P. Nordmann. 2006. Prevalence and genetic analysis of plasmid-mediated quinolone resistance determinants QnrA and QnrS in Enterobacteriaceae isolates from a French university hospital. Antimicrob. Agents Chemother. 50:3992-3997.[Abstract/Free Full Text]
    25. 25
  25. Robicsek, A., G. A. Jacoby, and D. C. Hooper. 2006. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect. Dis. 6:629-640.[CrossRef][Medline]
    26. 26
  26. Robicsek, A., J. Strahilevitz, G. A. Jacoby, M. Macielag, D. Abbanat, C. H. Park, K. Bush, and D. C. Hooper. 2006. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat. Med. 12:83-88.[CrossRef][Medline]
    27. 27
  27. Robicsek, A., J. Strahilevitz, D. F. Sahm, G. A. Jacoby, and D. C. Hooper. 2006. qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob. Agents Chemother. 50:2872-2874.[Abstract/Free Full Text]
    28. 28
  28. Rowe-Magnus, D. A., A. M. Guerout, P. Ploncard, B. Dychinco, J. Davies, and D. Mazel. 2001. The evolutionary history of chromosomal super-integrons provides an ancestry for multiresistant integrons. Proc. Natl. Acad. Sci. USA 98:652-657.[Abstract/Free Full Text]
    29. 29
  29. Shiraki, Y., N. Shibata, Y. Doi, and Y. Arakawa. 2004. Escherichia coli producing CTX-M-2 ß-lactamase in cattle, Japan. Emerg. Infect. Dis. 10:69-75.[Medline]
    30. 30
  30. Tran, J. H., and G. A. Jacoby. 2002. Mechanism of plasmid-mediated quinolone resistance. Proc. Natl. Acad. Sci. USA 99:5638-5642.[Abstract/Free Full Text]
    31. 31
  31. White, P. A., C. J. McIver, and W. D. Rawlinson. 2001. Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob. Agents Chemother. 45:2658-2661.[Abstract/Free Full Text]
    32. 32
  32. Wu, J.-J., W.-C. Ko, S.-H. Tsai, and J.-J. Yan. 2007. Prevalence of plasmid-mediated quinolone resistance determinants QnrA, QnrB, and QnrS among clinical isolates of Enterobacter cloacae in a Taiwanese hospital. Antimicrob. Agents Chemother. 51:1223-1227.[Abstract/Free Full Text]
    33. 33
  33. Zhao, S., S. Qaiyumi, S. Friedman, R. Singh, S. L. Foley, D. G. White, P. F. McDermott, T. Donkar, C. Bolin, S. Munro, E. J. Baron, and R. D. Walker. 2003. Characterization of Salmonella enterica serotype Newport isolated from humans and food animals. J. Clin. Microbiol. 41:5366-5371.[Abstract/Free Full Text]

Applied and Environmental Microbiology, October 2007, p. 6686-6690, Vol. 73, No. 20
0099-2240/07/$08.00+0     doi:10.1128/AEM.01054-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Strahilevitz, J., Jacoby, G. A., Hooper, D. C., Robicsek, A. (2009). Plasmid-Mediated Quinolone Resistance: a Multifaceted Threat. Clin. Microbiol. Rev. 22: 664-689 [Abstract] [Full Text]  
  • Ma, J., Zeng, Z., Chen, Z., Xu, X., Wang, X., Deng, Y., Lu, D., Huang, L., Zhang, Y., Liu, J., Wang, M. (2009). High Prevalence of Plasmid-Mediated Quinolone Resistance Determinants qnr, aac(6')-Ib-cr, and qepA among Ceftiofur-Resistant Enterobacteriaceae Isolates from Companion and Food-Producing Animals. Antimicrob. Agents Chemother. 53: 519-524 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ahmed, A. M.
Right arrow Articles by Shimamoto, T.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ahmed, A. M.
Right arrow Articles by Shimamoto, T.
Agricola
Right arrow Articles by Ahmed, A. M.
Right arrow Articles by Shimamoto, T.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»