Multidrug resistance genes in staphylococci from animals that confer resistance to critically and highly important antimicrobial agents in human medicine

Trends in Microbiology

Volumn 23, Issue 1, 2015, Pages 44-54

  Wendlandt, Sarah ^a   Shen, Jianzhong ^b   Kadlec, Kristina ^a   Wang, Yang ^b   Li, Beibei ^c   Zhang, Wan Jiang ^c   Feßler, Andrea T ^a   Wu, Congming ^b   Schwarz, Stefan ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Antimicrobial resistance; Colocation; Coselection; Cotransfer; Plasmid; Transposon

Indexed keywords

ABC TRANSPORTER; ANTIINFECTIVE AGENT; CLOXACILLIN; DALFOPRISTIN; DAPTOMYCIN; DICLOXACILLIN; FLUCLOXACILLIN; FUSIDIC ACID; LINEZOLID; NAFCILLIN; OXACILLIN; PRISTINAMYCIN; PSEUDOMONIC ACID; QUINUPRISTIN; RETAPAMULIN; TEICOPLANIN; TIAMULIN; TIGECYCLINE; VALNEMULIN; VANCOMYCIN; BACTERIAL PROTEIN; CFR PROTEIN, STAPHYLOCOCCUS AUREUS; VGA PROTEIN, STAPHYLOCOCCUS AUREUS;

ANIMAL; ANTIBIOTIC RESISTANCE; BACTERIAL GENE; CFR GENE; ERM GENE; GENE LOCATION; GENE SEQUENCE; GENE TARGETING; GENETIC SELECTION; GENETIC VARIABILITY; LSA(E) GENE; MDR GENE; MULTIDRUG RESISTANCE; NONHUMAN; PLASMID; REVIEW; STAPHYLOCOCCUS; TRANSPOSON; VGA GENE; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; STAPHYLOCOCCUS INFECTION; VETERINARY;

ANIMALIA; STAPHYLOCOCCUS;

ANIMALS; ANTI-BACTERIAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; HUMANS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS;

EID: 84920540267     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2014.10.002     Document Type: Review

References (100)

1. Nelson R. Antibiotic development pipeline runs dry. New drugs to fight resistant organisms are not being developed, experts say. Lancet 2003, 362:1726-1727.
2. Wenzel R.P. The antibiotic pipeline - challenges, costs, and values. N. Engl. J. Med. 2004, 351:523-526.
3. Shryock T.R., Richwine A. The interface between veterinary and human antibiotic use. Ann. N. Y. Acad. Sci. 2010, 1213:92-105.
4. Critically Important Antimicrobials for Human Medicine 2011, World Health Organization Advisory Group on Integrated Surveillance of Antimicrobial Resistance, World Health Organization.
5. Collignon P., et al. World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies for the use of antimicrobials in food production animals. Clin. Infect. Dis. 2009, 49:132-141.
6. Clinical and Laboratory Standards Institute (CLSI) Generation, presentation, and application of antimicrobial susceptibility test data for bacteria of animal origin; a report, CLSI document VET05-R 2011, Clinical and Laboratory Standards Institute.
7. Schwarz S., et al. Editorial: assessing the antimicrobial susceptibility of bacteria obtained from animals. J. Antimicrob. Chemother. 2010, 65:601-604.
8. Schwarz S., et al. Assessing the antimicrobial susceptibility of bacteria obtained from animals. Vet. Microbiol. 2010, 141:1-4.
9. Roberts M.C., et al. Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrob. Agents Chemother. 1999, 43:2823-2830.
10. Schwarz S., et al. Plasmid-mediated resistance to protein biosynthesis inhibitors in staphylococci. Ann. N. Y. Acad. Sci. 2011, 1241:82-103.
11. Wendlandt S., et al. The diversity of antimicrobial resistance genes among staphylococci of animal origin. Int. J. Med. Microbiol. 2013, 303:338-349.
12. Matsuoka M., et al. New erm gene in Staphylococcus aureus clinical isolates. Antimicrob. Agents Chemother. 2002, 46:211-215.
13. Kadlec K., et al. Diversity of antimicrobial resistance pheno- and genotypes of methicillin-resistant Staphylococcus aureus ST398 from diseased swine. J. Antimicrob. Chemother. 2009, 64:1156-1164.
14. Feßler A., et al. Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis. J. Antimicrob. Chemother. 2010, 65:619-625.
15. Entorf M., et al. Tylosin susceptibility of staphylococci from bovine mastitis. Vet. Microbiol. 2014, 171:368-373.
16. Feßler A.T., et al. Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl. Environ. Microbiol. 2011, 77:7151-7157.
17. Monecke S., et al. Genotyping of Staphylococcus aureus isolates from diseased poultry. Vet. Microbiol. 2013, 162:806-812.
18. Gharsa H., et al. High diversity of genetic lineages and virulence genes in nasal Staphylococcus aureus isolates from donkeys destined to food consumption in Tunisia with predominance of the ruminant associated CC133 lineage. BMC Vet. Res. 2012, 8:203.
19. Murphy E., et al. Transposon Tn554: complete nucleotide sequence and isolation of transposition-defective and antibiotic-sensitive mutants. EMBO J. 1985, 4:3357-3365.
20. Schwendener S., Perreten V. New transposon Tn6133 in methicillin-resistant Staphylococcus aureus ST398 contains vga(E), a novel streptogramin A, pleuromutilin, and lincosamide resistance gene. Antimicrob. Agents Chemother. 2011, 55:4900-4904.
21. Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements. Antimicrob. Agents Chemother. 2009, 53:4961-4967. International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC).
22. Wang X.M., et al. Methicillin-resistant Staphylococcus aureus ST9 from a case of bovine mastitis carries the genes cfr and erm(A) on a small plasmid. J. Antimicrob. Chemother. 2012, 67:1287-1289.
23. Argudín M.A., et al. Virulence and resistance determinants of German Staphylococcus aureus ST398 isolates from nonhuman sources. Appl. Environ. Microbiol. 2011, 77:3052-3060.
24. Walther B., et al. Comparative molecular analysis substantiates zoonotic potential of equine methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 2009, 47:704-710.
25. Lüthje P., Schwarz S. Molecular basis of resistance to macrolides and lincosamides among staphylococci and streptococci from various animal sources collected in the resistance monitoring program BfT-GermVet. Int. J. Antimicrob. Agents 2007, 29:528-535.
26. Eady E.A., et al. Distribution of genes encoding erythromycin ribosomal methylases and an erythromycin efflux pump in epidemiologically distinct groups of staphylococci. J. Antimicrob. Chemother. 1993, 31:211-217.
27. Werckenthin C., Schwarz S. Molecular analysis of the translational attenuator of a constitutively expressed erm(A) gene from Staphylococcus intermedius. J. Antimicrob. Chemother. 2000, 46:785-788.
28. Aarestrup F.M., et al. Antimicrobial susceptibility and presence of resistance genes in staphylococci from poultry. Vet. Microbiol. 2000, 74:353-364.
29. Jaglic Z., et al. Distribution, characterization and genetic bases of erythromycin resistance in staphylococci and enterococci originating from livestock. Zoonoses Public Health 2012, 59:202-211.
30. Shaw J.H., Clewell D.B. Complete nucleotide sequence of macrolide-lincosamide-streptogramin B-resistance transposon Tn917 in Streptococcus faecalis. J. Bacteriol. 1985, 164:782-796.
31. Wu S.W., et al. The Staphylococcus aureus transposon Tn551: complete nucleotide sequence and transcriptional analysis of the expression of the erythromycin resistance gene. Microb. Drug Resist. 1999, 5:1-7.
32. Boerlin P., et al. Molecular epidemiology and genetic linkage of macrolide and aminoglycoside resistance in Staphylococcus intermedius of canine origin. Vet. Microbiol. 2001, 79:155-169.
33. Kadlec K., et al. Molecular analysis of methicillin-resistant Staphylococcus pseudintermedius of feline origin from different European countries and North America. J. Antimicrob. Chemother. 2010, 65:1826-1828.
34. Perreten V., et al. Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. J. Antimicrob. Chemother. 2010, 65:1145-1154.
35. Gómez-Sanz E., et al. Detection and characterization of methicillin-resistant Staphylococcus pseudintermedius in healthy dogs in La Rioja, Spain. Comp. Immunol. Microbiol. Infect. Dis. 2011, 34:447-453.
36. Ben Zakour N.L., et al. Complete genome sequence of the canine pathogen Staphylococcus pseudintermedius. J. Bacteriol. 2011, 193:2363-2364.
37. Gómez-Sanz E., et al. Animal and human Staphylococcus aureus associated clonal lineages and high rate of Staphylococcus pseudintermedius novel lineages in Spanish kennel dogs: predominance of S. aureus ST398. Vet. Microbiol. 2012, 166:580-589.
38. Werckenthin C., et al. Macrolide-lincosamide-streptogramin B resistance in Staphylococcus lentus results from the integration of part of a transposon into a small plasmid. Antimicrob. Agents Chemother. 1996, 40:2224-2225.
39. Wang Y., et al. Distribution of the multidrug resistance gene cfr in Staphylococcus species isolates from swine farms in China. Antimicrob. Agents Chemother. 2012, 56:1485-1490.
40. Nawaz M.S., et al. Comparative molecular analysis of erythromycin-resistance determinants in staphylococcal isolates of poultry and human origin. Mol. Cell. Probes 2000, 14:311-319.
41. Lodder G., et al. Molecular analysis of naturally occurring ermC-encoding plasmids in staphylococci isolated from animals with and without previous contact with macrolide/lincosamide antibiotics. FEMS Immunol. Med. Microbiol. 1997, 18:7-15.
42. Strommenger B., et al. Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates. J. Antimicrob. Chemother. 2006, 57:461-465.
43. Coelho C., et al. Molecular detection and characterization of methicillin-resistant Staphylococcus aureus (MRSA) isolates from dogs in Portugal. Microb. Drug Resist. 2011, 17:333-337.
44. Gharsa H., et al. Prevalence, antibiotic resistance, virulence traits and genetic lineages of Staphylococcus aureus in healthy sheep in Tunisia. Vet. Microbiol. 2012, 156:367-373.
45. Vancraeynest D., et al. Antimicrobial resistance and resistance genes in Staphylococcus aureus strains from rabbits. Vet. Microbiol. 2004, 101:245-251.
46. Greene R.T., Schwarz S. Small antibiotic resistance plasmids in Staphylococcus intermedius. Zentralbl. Bakteriol. 1992, 276:380-389.
47. Schwarz S., et al. Plasmid-encoded resistance to macrolides and lincosamides in Staphylococcus hyicus. J. Appl. Bacteriol. 1990, 69:845-849.
48. Schwarz S., et al. Molecular analysis of the macrolide-lincosamide resistance gene region of a novel plasmid from Staphylococcus hyicus. J. Med. Microbiol. 1998, 47:63-70.
49. Hauschild T., et al. Staphylococcal tetracycline-MLSB resistance plasmid pSTE2 is the product of an RSA-mediated in vivo recombination. J. Antimicrob. Chemother. 2005, 56:399-402.
50. Diep B.A., et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 2006, 367:731-739.
51. Gómez-Sanz E., et al. Novel erm(T)-carrying multiresistance plasmids from porcine and human isolates of methicillin-resistant Staphylococcus aureus ST398 that also harbor cadmium and copper resistance determinants. Antimicrob. Agents Chemother. 2013, 57:3275-3282.
52. Chung W.O., et al. Host range of the ermF rRNA methylase gene in bacteria of human and animal origin. J. Antimicrob. Chemother. 1999, 43:5-14.
53. Kadlec K., Schwarz S. Identification of a plasmid-borne resistance gene cluster comprising the resistance genes erm(T), dfrK, and tet(L) in a porcine methicillin-resistant Staphylococcus aureus ST398 strain. Antimicrob. Agents Chemother. 2010, 54:915-918.
54. Schwarz S., et al. Staphylococcus sciuri gene erm(33), encoding inducible resistance to macrolides, lincosamides, and streptogramin B antibiotics, is a product of recombination between erm(C) and erm(A). Antimicrob. Agents Chemother. 2002, 46:3621-3623.
55. Schwendener S., Perreten V. New MLSB resistance gene erm(43) in Staphylococcus lentus. Antimicrob. Agents Chemother. 2012, 56:4746-4752.
56. Wendlandt S., et al. The enterococcal ABC transporter gene lsa(E) confers combined resistance to lincosamides, pleuromutilins and streptogramin A antibiotics in methicillin-susceptible and methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 2013, 68:473-475.
57. Kadlec K., et al. Novel and uncommon antimicrobial resistance genes in livestock-associated methicillin-resistant Staphylococcus aureus. Clin. Microbiol. Infect. 2012, 18:745-755.
58. Overesch G., et al. The increase of methicillin-resistant Staphylococcus aureus (MRSA) and the presence of an unusual sequence type ST49 in slaughter pigs in Switzerland. BMC Vet. Res. 2011, 7:30.
59. Lozano C., et al. Identification of novel vga(A)-carrying plasmids and a Tn5406-like transposon in meticillin-resistant Staphylococcus aureus and Staphylococcus epidermidis of human and animal origin. Int. J. Antimicrob. Agents 2012, 40:306-312.
60. Weiß S., et al. Complete sequence of a multiresistance plasmid from a methicillin-resistant Staphylococcus epidermidis ST5 isolated in a small animal clinic. J. Antimicrob. Chemother. 2014, 69:847-849.
61. Kadlec K., Schwarz S. Identification of a novel ABC transporter gene, vga(C), located on a multiresistance plasmid from a porcine methicillin-resistant Staphylococcus aureus ST398 strain. Antimicrob. Agents Chemother. 2009, 53:3589-3591.
62. Kadlec K., et al. Small plasmids carrying vga(A) or vga(C) genes mediate resistance to lincosamides, pleuromutilins and streptogramin A antibiotics in methicillin-resistant Staphylococcus aureus ST398 from swine. J. Antimicrob. Chemother. 2010, 65:2692-2693.
63. Hauschild T., et al. Detection of the novel vga(E) gene in methicillin-resistant Staphylococcus aureus CC398 isolates from cattle and poultry. J. Antimicrob. Chemother. 2012, 67:503-504.
64. Li J., et al. Identification of a novel vga(E) gene variant that confers resistance to pleuromutilins, lincosamides and streptogramin A antibiotics in staphylococci of porcine origin. J. Antimicrob. Chemother. 2014, 69:919-923.
65. Kehrenberg C., et al. Nucleotide sequence and organization of the multiresistance plasmid pSCFS1 from Staphylococcus sciuri. J. Antimicrob. Chemother. 2004, 54:936-939.
66. Li B., et al. Detection and new genetic environment of the pleuromutilin-lincosamide-streptogramin A resistance gene lsa(E) in methicillin-resistant Staphylococcus aureus of swine origin. J. Antimicrob. Chemother. 2013, 68:1251-1255.
67. Wendlandt S., et al. Complete sequence of the multi-resistance plasmid pV7037 from a porcine methicillin-resistant Staphylococcus aureus. Vet. Microbiol. 2013, 166:650-654.
68. Wendlandt S., et al. Enterococcal multiresistance gene cluster in methicillin-resistant Staphylococcus aureus from various origins and geographical locations. J. Antimicrob. Chemother. 2014, 69:2573-2575.
69. Kehrenberg C., et al. A new mechanism for chloramphenicol, florfenicol and clindamycin resistance: methylation of 23S ribosomal RNA at A2503. Mol. Microbiol. 2005, 57:1064-1073.
70. Long K.S., et al. The Cfr rRNA methyltransferase confers resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A antibiotics. Antimicrob. Agents Chemother. 2006, 50:2500-2505.
71. Schwarz S., et al. Identification of a plasmid-borne chloramphenicol-florfenicol resistance gene in Staphylococcus sciuri. Antimicrob. Agents Chemother. 2000, 44:2530-2533.
72. Kehrenberg C., Schwarz S. Distribution of florfenicol resistance genes fexA and cfr among chloramphenicol-resistant Staphylococcus isolates. Antimicrob. Agents Chemother. 2006, 50:1156-1163.
73. Vanderhaeghen W., et al. Characterization of methicillin-resistant non-Staphylococcus aureus staphylococci carriage isolates from different bovine populations. J. Antimicrob. Chemother. 2013, 68:300-307.
74. Kehrenberg C., et al. IS21-558 insertion sequences are involved in the mobility of the multiresistance gene cfr. Antimicrob. Agents Chemother. 2007, 51:483-487.
75. Kehrenberg C., et al. Methicillin-resistant and -susceptible Staphylococcus aureus strains of clonal lineages ST398 and ST9 from swine carry the multidrug resistance gene cfr. Antimicrob. Agents Chemother. 2009, 53:779-781.
76. Wang Y., et al. Multidrug resistance gene cfr in methicillin-resistant coagulase-negative staphylococci from chickens, ducks, and pigs in China. Int. J. Med. Microbiol. 2013, 303:84-87.
77. He T., et al. Genetic environment of the multi-resistance gene cfr in methicillin-resistant coagulase-negative staphylococci from chickens, ducks, and pigs in China. Int. J. Med. Microbiol. 2014, 304:257-261.
78. Shen J., et al. Presence and dissemination of the multiresistance gene cfr in Gram-positive and Gram-negative bacteria. J. Antimicrob. Chemother. 2013, 68:1697-1706.
79. Lyon B.R., Skurray R. Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol. Rev. 1987, 51:88-134.
80. Jensen S.O., Lyon B.R. Genetics of antimicrobial resistance in Staphylococcus aureus. Future Microbiol. 2009, 4:565-582.
81. Grave K., et al. Comparison of the sales of veterinary antibacterial agents between 10 European countries. J. Antimicrob. Chemother. 2010, 65:2037-2040.
82. Hansen L.H., et al. The order Bacillales hosts functional homologs of the worrisome cfr antibiotic resistance gene. Antimicrob. Agents Chemother. 2012, 56:3563-3567.
83. Allignet J., El Solh N. Comparative analysis of staphylococcal plasmids carrying three streptogramin-resistance genes: vat-vgb-vga. Plasmid 1999, 42:134-138.
84. Gentry D.R., et al. Genetic characterization of Vga ABC proteins conferring reduced susceptibility of Staphylococcus aureus to pleuromutilins. Antimicrob. Agents Chemother. 2008, 52:4507-4509.
85. Haroche J., et al. Characterization of a variant of vga(A) conferring resistance to streptogramin A and related compounds. Antimicrob. Agents Chemother. 2000, 44:2271-2275.
86. Locke J.B., et al. Identification and characterization of linezolid-resistant USA300 Staphylococcus aureus isolates from a New York City medical center possessing the cfr multidrug resistance gene. Antimicrob Agents Chemother. 2014, 58:6949-6952.
87. LaMarre J., et al. The genetic environment of the cfr gene and the presence of other mechanisms account for the very high linezolid resistance of Staphylococcus epidermidis isolate 426-3147L. Antimicrob. Agents Chemother. 2013, 57:1173-1179.
88. Cui L., et al. Cfr-mediated linezolid-resistance among methicillin-resistant coagulase-negative staphylococci from infections of humans. PLoS ONE 2013, 8:e57096.
89. Feßler A.T., et al. Cfr-mediated linezolid resistance in methicillin-resistant Staphylococcus aureus and Staphylococcus haemolyticus associated with clinical infections in humans: two case reports. J. Antimicrob. Chemother. 2014, 69:268-270.
90. Mendes R.E., et al. Dissemination of a pSCFS3-like cfr-carrying plasmid in Staphylococcus aureus and Staphylococcus epidermidis clinical isolates recovered from hospitals in Ohio. Antimicrob. Agents Chemother. 2013, 57:2923-2928.
91. Shore A.C., et al. Identification and characterization of the multidrug resistance gene cfr in a Panton-Valentine leukocidin-positive sequence type 8 methicillin-resistant Staphylococcus aureus IVa (USA300) isolate. Antimicrob. Agents Chemother. 2010, 54:4978-4984.
92. Liu Y., et al. First report of multiresistance gene cfr in Enterococcus species casseliflavus and gallinarum of swine origin. Vet. Microbiol. 2014, 170:352-357.
93. Wang Y., et al. First report of the multiresistance gene cfr in Streptococcus suis. Antimicrob. Agents Chemother. 2013, 57:4061-4063.
94. Liu Y., et al. Investigation of a multiresistance gene cfr that fails to mediate resistance to phenicols and oxazolidinones in Enterococcus faecalis. J. Antimicrob. Chemother. 2014, 69:892-898.
95. Liu Y., et al. Transferable multiresistance plasmids carrying cfr in Enterococcus spp. from swine and farm environment. Antimicrob. Agents Chemother. 2013, 57:42-48.
96. Diaz L., et al. Transferable plasmid-mediated resistance to linezolid due to cfr in a human clinical isolate of Enterococcus faecalis. Antimicrob. Agents Chemother. 2012, 56:3917-3922.
97. Wang Y., et al. Detection of the staphylococcal multiresistance gene cfr in Macrococcus caseolyticus and Jeotgalicoccus pinnipedialis. J. Antimicrob. Chemother. 2012, 67:1824-1827.
98. Zhang W.J., et al. Characterization of the IncA/C plasmid pSCEC2 from Escherichia coli of swine origin that harbours the multiresistance gene cfr. J. Antimicrob. Chemother. 2014, 69:385-389.
99. Deng H., et al. Identification of the multi-resistance gene cfr in Escherichia coli isolates of animal origin. PLoS ONE 2014, 9:e102378.
100. Wang Y., et al. Detection of the staphylococcal multiresistance gene cfr in Escherichia coli of domestic-animal origin. J. Antimicrob. Chemother. 2012, 67:1094-1098.