Role of the Environment in the Transmission of Antimicrobial Resistance to Humans: A Review

Environmental Science and Technology

Volumn 49, Issue 20, 2015, Pages 11993-12004

  Huijbers, Patricia M C ^a,b   Blaak, Hetty ^b   De Jong, Mart C M ^a   Graat, Elisabeth A M ^a   Vandenbroucke Grauls, Christina M J E ^c   De Roda Husman, Ana Maria ^b,d  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

POTABLE WATER;

ANTIMICROBIAL RESISTANCES; CONTAMINATION SOURCES; ENVIRONMENTAL COMPARTMENT; INTERVENTION STRATEGY; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; NATURAL ENVIRONMENTS; TEMPORAL RELATIONSHIPS; VANCOMYCIN-RESISTANT ENTEROCOCCI;

BACTERIA;

DRINKING WATER; WATER; ANTIINFECTIVE AGENT; BETA LACTAMASE; MANURE;

AMBIENT AIR; ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BACTERIUM; DATA SET; DRINKING WATER; MANURE; OCCUPATIONAL EXPOSURE; PUBLIC HEALTH; QUANTITATIVE ANALYSIS; RISK ASSESSMENT; SHELLFISH; WASTEWATER;

AIR; AMBIENT AIR; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL TRANSMISSION; BACTERIUM CONTAMINATION; BACTERIUM DETECTION; DUST; ENVIRONMENT; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ENTEROBACTERIACEAE; HUMAN; MANURE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; RECREATION; SHELLFISH; SOIL; VANCOMYCIN RESISTANT ENTEROCOCCUS; WASTE WATER; WILDLIFE; ANIMAL; BACTERIUM; DRUG EFFECTS; ENTEROBACTERIACEAE; FECES; FOOD CONTROL; ISOLATION AND PURIFICATION; META ANALYSIS; METABOLISM; MICROBIOLOGY;

ENTEROBACTERIACEAE; ENTEROCOCCUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BETA-LACTAMASES; DRUG RESISTANCE, BACTERIAL; ENTEROBACTERIACEAE; ENVIRONMENT; FECES; FOOD MICROBIOLOGY; HUMANS; MANURE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; RECREATION; SOIL MICROBIOLOGY; VANCOMYCIN-RESISTANT ENTEROCOCCI; WATER MICROBIOLOGY;

EID: 84945282416     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b02566     Document Type: Article

References (60)

1. World Health Organization (WHO). Antimicrobial resistance: global report on surveillance; World Health Organization: Geneva, Switzerland, 2014; http://www.who.int/drugresistance/documents/surveillancereport/en/ (accessed Sept 3, 2015).
2. de Kraker, M. E. A.; Davey, P. G.; Grundmann, H. Mortality and hospital stay associated with resistant Staphylococcus aureus and Escherichia coli bacteraemia: Estimating the burden of antimicrobial resistance in Europe PLoS Med. 2011, 8, e1001104 10.1371/journal.pmed.1001104
3. Pires, S. M.; Evers, E. G.; van Pelt, W.; Ayers, T.; Scallan, E.; Angulo, F. J.; Havelaar, A.; Hald, T. Attributing the human disease burden of foodborne infections to specific sources Foodborne Pathog. Dis. 2009, 6, 417-424 10.1089/fpd.2008.0208
4. Domingues, A. R.; Pires, S. M.; Halasa, T.; Hald, T. Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections Epidemiol. Infect. 2012, 140, 970-981 10.1017/S0950268811002676
5. Domingues, A. R.; Pires, S. M.; Halasa, T.; Hald, T. Source attribution of human salmonellosis using a meta-analysis of case-control studies of sporadic infections Epidemiol. Infect. 2012, 140, 959-969 10.1017/S0950268811002172
6. Evers, E. G.; van der Vels-Klerx, H. J.; Nauta, M. J.; Schijven, J. F.; Havelaar, A. H. Campylobacter source attribution by exposure assessment Int. J. Risk Assess. Manage. 2008, 8, 174-189 10.1504/IJRAM.2008.016151
7. Rangel, J. M.; Sparling, P. H.; Crowe, C.; Griffin, P. M.; Swerdlow, D. L. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002 Emerging Infect. Dis. 2005, 11, 603-609 10.3201/eid1104.040739
8. Shuval, H. Estimating the global burden of thalassogenic diseases: human infectious diseases caused by wastewater pollution of the marine environment J. Water Health 2003, 1, 53-64
9. Franz, E.; van Bruggen, A. H. Ecology of E. coli O157:H7 and Salmonella enterica in the primary vegetable production chain Crit. Rev. Microbiol. 2008, 34, 143-161 10.1080/10408410802357432
10. Centres for Disease Control and Prevention (CDC) Outbreak of Escherichia coli O104:H4 infections associated with sprout consumption-Europe and North America, May-July 2011 Morbidity Mortality Weekly Rep. 2013, 62, 1029-1031
11. Centers for Disease Control and Prevention (CDC) Ongoing multistate outbreak of Escherichia coli serotype O157:H7 infections associated with consumption of fresh spinach-United States, September 2006 Morbidity Mortality Weekly Rep. 2006, 55, 1-2
12. Davies, J.; Davies, J. Origins and evolution of antibiotic resistance Microbiol. Mol. Biol. Rev. 2010, 74, 417-433 10.1128/MMBR.00016-10
13. Clinical Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing, 20th Informational Supplement M100-20; Clinical Laboratory Standards Institute: Wayne, PA, 2010.
14. Centers for Disease Control and Prevention (CDC). Vancomycin-resistant Enterococci (VRE) and the clinical laboratory; Centres for Disease Control and Prevention: Atlanta, GA, 2010; http://www.cdc.gov/HAI/settings/lab/VREClinical-Laboratory.html (accessed Sept 3, 2015).
15. Blaak, H.; de Kruijf, P.; Hamidjaja, R. A.; van Hoek, A. H. A. M.; de Roda Husman, A. M.; Schets, F. M. Prevalence and characteristics of ESBL-producing E. coli in Dutch recreational waters influenced by wastewater treatment plants Vet. Microbiol. 2014, 171, 448-459 10.1016/j.vetmic.2014.03.007
16. Goodwin, K. D.; McNay, M.; Cao, Y.; Ebentier, D.; Madison, M.; Griffith, J. F. A multi-beach study of Staphylococcus aureus, MRSA, and Enterococci in seawater and beach sand Water Res. 2012, 46, 4195-4207 10.1016/j.watres.2012.04.001
17. Levin-Edens, E.; Soge, O. O.; No, D.; Stiffarm, A.; Meschke, J. S.; Roberts, M. C. Methicillin-resistant Staphylococcus aureus from Northwest marine and freshwater recreational beaches FEMS Microbiol. Ecol. 2012, 79, 412-420 10.1111/j.1574-6941.2011.01229.x
18. Plano, L. R. W.; Shibata, T.; Garza, A. C.; Kish, J.; Fleisher, J. M.; Sinigalliano, C. D.; Gidley, M. L.; Withum, K.; Elmir, S. M.; Hower, S.; Jackson, C. R.; Barret, J. B.; Cleary, T.; Davidson, M.; Mukherjee, S.; Fleming, L. E.; Solo-Gabriele, H. M. Human-associated methicillin-resistant Staphylococcus aureus from a subtropical recreational marine beach Microb. Ecol. 2013, 65, 1039-1051 10.1007/s00248-013-0216-1
19. Guardabassi, L.; Dalsgaard, A. Occurrence, structure, and mobility of Tn1546-like elements in environmental isolates of vancomycin-resistant Enterococci Appl. Environ. Microbiol. 2004, 70, 984-990 10.1128/AEM.70.2.984-990.2004
20. Hower, S.; Phillips, M. C.; Brodsky, M.; Dameron, A.; Tamargo, M. A.; Salazar, N. C.; Jackson, C. R.; Barrett, J. B.; Davidson, M.; Davis, J.; Mukherjee, S.; Ewing, R. Y.; Gidley, M. L.; Sinigalliano, C. D.; Johns, L.; Johnson, F. E.; Adebanjo, O.; Plano, L. R. Clonally related methicillin-resistant Staphylococcus aureus isolated from short-finned pilot whales (Globicephala macrorhynchus), human volunteers, and a bayfront cetacean rehabilitation facility Microb. Ecol. 2013, 65, 1024-1038 10.1007/s00248-013-0178-3
21. Doljeská, M.; Biero͉ová, B.; Kohoutová, L.; Litarák, I.; ɤížek, A. Antibiotic-resistant Salmonella and Escherichia coli isolates with integrons and extended-spectrum beta-lactamases in surface water and sympatric black-headed gulls J. Appl. Microbiol. 2009, 106, 1941-1950 10.1111/j.1365-2672.2009.04155.x
22. Hernández, J.; Stedt, J.; Bonnedahl, J.; Molin, Y.; Drobni, M.; Calisto-Ulloa, N.; Gomez-Fuentes, C.; Astorga-España, M. S.; González-Acuña, D.; Waldenström, J.; Blomqvist, M.; Olsen, B. Human-associated extended-spectrum β-lacatamase in the Antarctic Appl. Environ. Microbiol. 2012, 78, 2056-2058 10.1128/AEM.07320-11
23. Alouache, S.; Estepa, V.; Messai, Y.; Ruiz, E.; Torres, C.; Bakour, R. Characterization of ESBLs and associated quinolone resistance in Escherichia coli and Klebsiella pneumoniae isolates from an urban wastewater treatment plant in Algeria Microb. Drug Resist. 2014, 20, 30-38 10.1089/mdr.2012.0264
24. Gómez, M.; Díaz, M. T.; Araujo, M.; Sueiro, R.; Garrido, J. Waste water treatment plants as redistributors of resistance genes in bacteria WIT Trans. Ecol. Environ. 2010, 135, 83-94 10.2495/WP100081
25. Guardabassi, L.; Brønnum, P. T.; Danø, R.; Forslund, A.; Dalsgaard, A. Dissemination of vancomycin-resistant Enterococci harboring vanA through disposal of waste derived from industrial production of vancomycin Microb. Drug Resist. 2002, 8, 401-406 10.1089/10766290260469688
26. Nagulapally, S. R.; Ahmad, A.; Henry, A.; Marchin, G. L.; Zurek, L.; Bhandari, A. Occurrence of ciprofloxacin-, trimethoprim-sulfamethoxazole-, and vancomycin-resistant bacteria in a municipal wastewater treatment plant Water Environ. Res. 2009, 81, 82-90 10.2175/106143008X304596
27. Rosenberg Goldstein, R. E.; Micallef, S. A.; Gibbs, S. G.; George, A.; Claye, E.; Sapkota, A.; Joseph, S. W.; Sapkota, A. R. Detection of vancomycin-resistant Enterococci (VRE) at four U.S. wastewater treatment plants that provide effluent for reuse Sci. Total Environ. 2014, 466-467, 404-411 10.1016/j.scitotenv.2013.07.039
28. Varela, A. R.; Ferro, G.; Vredenburg, J.; Yanik, M.; Vieira, L.; Rizzo, L.; Lameiras, C.; Manaia, C. M. Vancomycin resistant Enterococci: from the hospital effluent to the urban wastewater treatment plant Sci. Total Environ. 2013, 450-451, 155-161 10.1016/j.scitotenv.2013.02.015
29. Blanch, A. R.; Caplin, J. L.; Iversen, A.; Kühn, I.; Manero, A.; Taylor, H. D.; Vilanova, X. Comparison of enterococcal populations related to urban and hospital wastewater in various climatic and geographic European regions J. Appl. Microbiol. 2003, 94, 994-1002 10.1046/j.1365-2672.2003.01919.x
30. Korzeniewska, E.; Korzeniewska, A.; Harnisz, M. Antibiotic resistant Escherichia coli in hospital and municipal sewage and their emission to the environment Ecotoxicol. Environ. Saf. 2013, 91, 96-102 10.1016/j.ecoenv.2013.01.014
31. Korzeniewska, E.; Harnisz, M. Extended-spectrum beta-lactamase (ESBL)-positive Enterobacteriaceae in municipal sewage and their emission to the environment J. Environ. Manage. 2013, 128, 904-911 10.1016/j.jenvman.2013.06.051
32. Kühn, I.; Iversen, A.; Finn, M.; Greko, C.; Burman, L. G.; Blanch, A. R.; Vilanova, X.; Manero, A.; Taylor, H.; Caplin, J.; Domínguez, L.; Herrero, I. A.; Moreno, M. A.; Möllby, R. Occurrence and relatedness of vancomycin-resistant Enterococci in animals, humans, and the environment in different European regions Appl. Environ. Microbiol. 2005, 71, 5383-5390 10.1128/AEM.71.9.5383-5390.2005
33. Novais, C.; Coque, T. M.; Ferreira, H.; Sousa, J. C.; Peixe, L. Environmental contamination with vancomycin-resistant Enterococci from hospital sewage in Portugal Appl. Environ. Microbiol. 2005, 71, 3364-3368 10.1128/AEM.71.6.3364-3368.2005
34. Schwartz, T.; Kohnen, W.; Jansen, B.; Obst, U. Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms FEMS Microbiol. Ecol. 2003, 43, 325-335 10.1111/j.1574-6941.2003.tb01073.x
35. Friese, A.; Schulz, J.; Laube, H.; von Salviati, C.; Hartung, J.; Roesler, U. Faecal occurrence and emissions of livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) and ESBL/AmpC-producing E. coli from animal farms in Germany Berl. Münch. Tierärztl. Wochenschr. 2013, 126, 175-180 10.2376/0005-9366-126-17
36. Hartmann, A.; Locatelli, A.; Amoureux, L.; Depret, G.; Jolivet, C.; Gueneau, E.; Neuwirth, C. Occurrence of CTX-M producing Escherichia coli in soils, cattle, and farm environment in France (Burgundy region) Front. Microbiol. 2012, 3, e83 10.3389/fmicb.2012.00083
37. Hasan, B.; Sandegren, L.; Melhus, Å.; Drobni, M.; Hernández, J.; Waldenström, J.; Alam, M.; Olsen, B. Antimicrobial drug-resistant Escherichia coli in wild birds and free-range poultry, Bangladesh Emerging Infect. Dis. 2012, 18, 2055-2058 10.3201/eid1812.120513
38. Ma, J.; Liu, J. H.; Lv, L.; Zong, Z.; Sun, Y.; Zheng, H.; Chen, Z.; Zeng, Z. L. Characterization of extended-spectrum β-lactamase genes found among Escherichia coli isolates from duck and environmental samples obtained on a duck farm Appl. Environ. Microbiol. 2012, 78, 3668-3673 10.1128/AEM.07507-11
39. Manero, A.; Vilanova, X.; Cerdà-Cuéllar, M.; Blanch, A. R. Vancomycin- and erythromycin-resistant Enterococci in a pig farm and its environment Environ. Microbiol. 2006, 8, 667-674 10.1111/j.1462-2920.2005.00945.x
40. Ashbolt, N. J.; Amézquita, A.; Backhaus, T.; Borriello, P.; Brandt, K. K.; Collignon, P.; Coors, A.; Finley, R.; Gaze, W. H.; Heberer, T.; Lawrence, J. R.; Larsson, D. G. J.; McEwen, S. A.; Ryan, J. J.; Schönfeld, J.; Silley, P.; Snape, J. R.; van den Eede, C.; Topp, E. Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance Environ. Health Perspect. 2013, 121, 993-1001 10.1289/ehp.1206316
41. Hunter, P. R.; Wilkinson, D. C.; Catling, L. A.; Barker, G. C. Meta-analysis of experimental data concerning antimicrobial resistance gene transfer rates during conjugation Appl. Environ. Microbiol. 2008, 74, 6085-6090 10.1128/AEM.01036-08
42. Harwood, V. J.; Staley, C.; Badgley, B. D.; Borges, K.; Korajkic, A. Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens and human health outcomes FEMS Microbiol. Rev. 2014, 38, 1-40 10.1111/1574-6976.12031
43. Sabat, A. J.; Budimir, A.; Nashev, D.; Sá-Leão, R.; van Dijl, J. M.; Laurent, F.; Grundmann, H.; Friedrich, A. W. Overview of molecular typing methods for outbreak detection and epidemiological surveillance Euro Surveill. 2013, 18, 20380
44. (http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20380, accessed Sept 3, 2015)
45. Dröge, M.; Pühler, A.; Selbitschka, W. Horizontal gene transfer among bacteria in terrestrial and aquatic habitats as assessed by microcosm studies Biol. Fertil. Soils 1999, 29, 221-245 10.1007/s003740050548
46. Monier, J. M.; Demanèche, S.; Delmont, T. O.; Mathieu, A.; Vogel, T. M.; Simonet, P. Metagenomic exploration of antibiotic resistance in soil Curr. Opin. Microbiol. 2011, 14, 229-235 10.1016/j.mib.2011.04.010
47. Frank, C.; Werber, D.; Cramer, J. P.; Askar, M.; Faber, M.; an der Heiden, M.; Bernard, H.; Fruth, A.; Prager, R.; Spode, A.; Wadl, M.; Zoufaly, A.; Jordan, S.; Kemper, M. J.; Follin, P.; Müller, L.; King, L. A.; Rosner, B.; Buchholz, U.; Stark, K.; Krause, G. Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany N. Engl. J. Med. 2011, 365, 1771-1780 10.1056/NEJMoa1106483
48. Buchholz, U.; Bernard, H.; Werber, D.; Böhmer, M. M.; Remschmidt, C.; Wilking, H.; Deleré, Y.; an der Heiden, M.; Adlhoch, C.; Dreesman, J.; Ehlers, J.; Ethelberg, S.; Faber, M.; Frank, C.; Fricke, G.; Greiner, M.; Höhle, M.; Ivarsson, S.; Jark, U.; Kirchner, M.; Koch, J.; Krause, G.; Luber, P.; Rosner, B.; Stark, K.; Kühne, M. German outbreak of Escherichia coli O104:H4 associated with sprouts N. Engl. J. Med. 2011, 365, 1763-1770 10.1056/NEJMoa1106482
49. Søraas, A.; Sundsfjord, A.; Sandven, I.; Brunborg, C.; Jenum, P. A. Risk factors for community-acquired urinary tract infections caused by ESBL-producing Enterobacteriaceae-A case-control study in a low prevalence country PLoS One 2013, 8, e69581 10.1371/journal.pone.0069581
50. Huijbers, P. M. C.; de Kraker, M.; Graat, E. A. M.; van Hoek, A. H. A. M.; van Santen, M. G.; de Jong, M. C. M.; van Duijkeren, E.; de Greeff, S. C. Prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in humans living in municipalities with high and low broiler density Clin. Microbiol. Infect. 2013, 19, E256-E259 10.1111/1469-0691.12150
51. Rosenberg Goldstein, R. E.; Micallef, S. A.; Gibbs, S. G.; He, X.; George, A.; Sapkota, A.; Joseph, S. W.; Sapkota, A. R. Occupational exposure to Staphylococcus aureus and Enterococcus spp. among spray irrigation worker using reclaimed water Int. J. Environ. Res. Public Health 2014, 11, 4340-4355 10.3390/ijerph110404340
52. Fahrenfeld, N.; Knowlton, K.; Krometis, L. A.; Hession, W. C.; Xia, K.; Lipscomb, E.; Libuit, K.; Green, B. L.; Pruden, A. Effect of manure application on abundance of antibiotic resistance genes and their attenuation rates in soil: Field-scale mass balance approach Environ. Sci. Technol. 2014, 48, 2643-2650 10.1021/es404988k
53. Chee-Sanford, J. C.; Mackie, R. I.; Koike, S.; Krapac, I. G.; Lin, Y. F.; Yannarell, A. C.; Maxwell, S.; Aminov, R. I. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste J. Environ. Qual. 2009, 38, 1086-1108 10.2134/jeq2008.0128
54. Pruden, A.; Larsson, D. G. J.; Amézquita, A.; Collignon, P.; Brandt, K. K.; Graham, D. W.; Lazorchak, J. M.; Suzuki, S.; Silley, P.; Snape, J. R.; Topp, E.; Zhang, T.; Zhu, Y. G. Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment Environ. Health. Perspect. 2013, 121, 878-885 10.1289/ehp.1206446
55. Krüger, U. Membrane-supported biological wastewater treatment Schriftenr. Ver. Wasser. Boden Lufthyg. 2000, 105, 319-324
56. Friese, A.; Schulz, J.; Zimmermann, K.; Tenhagen, B. A.; Fetsch, A.; Hartung, J.; Rösler, U. Occurrence of livestock-associated methicillin-resistant Staphylococcus aureus in turkey and broiler barns and contamination of air and soil surfaces in their vicinity Appl. Environ. Microbiol. 2013, 79, 2759-2766 10.1128/AEM.03939-12
57. Clauss, M.; Schulz, J.; Stratmann-Selke, J.; Decius, M.; Hartung, J. Reduction of livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) in the exhaust air of two piggeries by a bio-trickling filter and a biological three-step air cleaning system Berl. Münch. Tierärztl. Wochenschr. 2013, 126, 137-142
58. Blaak, H.; Hamidjaja, R. A.; van Hoek, A. H. A. M.; de Heer, L.; de Roda Husman, A. M.; Schets, F. M. Detection of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli on flies at poultry farms Appl. Environ. Microbiol. 2014, 80, 239-246 10.1128/AEM.02616-13
59. Korzeniewska, E.; Harnisz, M. Beta-lactamase-producing Enterobacteriaceae in hospital effluents J. Environ. Manage. 2013, 123, 1-7 10.1016/j.jenvman.2013.03.024
60. Bates, J.; Jordens, J. Z.; Griffiths, D. T. Farm animals given as a putative reservoir for vancomycin-resistant enterococcal infection in man J. Antimicrob. Chemother. 1994, 34, 507-514 10.1093/jac/34.4.507