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, , , , , , , , , , , , , , , , , and
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Reference Manager
BibTeX
Zotero
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Wellington EMH et al. 2013. The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect Dis 13: 155–165.
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Gao X, Shao M, Luo Y, Dong Y, Ouyang F, Dong W, Li J, 2016. Airborne bacterial contaminations in typical Chinese wet market with live poultry trade. Sci Total Environ 572: 681–687.
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Echeverria-Palencia CM et al. 2017. Disparate antibiotic resistance gene quantities revealed across 4 major cities in California: a survey in drinking water, air, and soil at 24 public parks. ACS Omega 2: 2255–2263.
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Sancheza HM et al. 2016. Antibiotic resistance in airborne bacteria near conventional and organic beef cattle farms in California, USA. Water Air Soil Pollut: 227–280. doi: 10.1007/s11270-016-2979-8.
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16.
Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D, 2013. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447: 345–360.
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17.
Liu D et al. 2012. Formation and transmission of Staphylococcus aureus (including MRSA) aerosols carrying antibiotic-resistant genes in a poultry farming environment. Sci Total Environ 426: 139–145.
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18.
McEachran AD, Blackwell BR, Hanson JD, Wooten KJ, Mayer GD, Cox SB, Smith PN, 2015. Antibiotics, bacteria, and antibiotic resistance genes: aerial transport from cattle feed yards via particulate matter. Environ Health Perspect 123: 337–343.
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Hu J, Zhao F, Zhang XX, Li K, Li C, Ye L, Li M, 2018. Metagenomic profiling of ARGs in airborne particulate matters during a severe smog event. Sci Total Environ 615: 1332–1340.
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Li J et al. 2018. Global survey of antibiotic resistance genes in air. Environ Sci Technol 52: 10975–10984.
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Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM, 2013. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA 110: 3435–3440.
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Zhang M, Zuo J, Yu X, Shi X, Chen L, Li Z, 2017. Quantification of multi-antibiotic resistant opportunistic pathogenic bacteria in bioaerosols in and around a pharmaceutical wastewater treatment plant. J Environ Sci 72: 53–63.
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Gao M, Qiu T, Sun Y, Wang X, 2018. The abundance and diversity of antibiotic resistance genes in the atmospheric environment of composting plants. Environ Int 116: 229–238.
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Gibbs SG, Green CF, Tarwater PM, Mota LC, Mena KD, Scarpino PV, 2006. Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environ Health Perspect 114: 1032–1037.
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Hyvärinen AP, Raatikainen T, Brus D, Komppula M, Panwar TS, Hooda RK, Sharma VP, Lihavainen H, 2011. Effect of the summer monsoon on aerosols at two measurement stations in Northern India–Part 1: PM and BC concentrations. Atmos Chem Phys 11: 8271–8282.
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Open Waste Canals as Potential Sources of Antimicrobial Resistance Genes in Aerosols in Urban Kanpur, India
Olivia Ginn
Olivia Ginn
School of Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, Georgia;
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David Berendes
David Berendes
Department of Epidemiology, Rollins School of Public Health, Emory University, Atlanta, Georgia;
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Anna Wood
Anna Wood
Department of Civil and Environmental Engineering and Earth Science, University of Notre Dame, Notre Dame, Indiana;
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Aaron Bivins
Aaron Bivins
Department of Civil and Environmental Engineering, Duke Global Health Institute, Duke University, Durham, North Carolina;
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Lucas Rocha-Melogno
Lucas Rocha-Melogno
Department of Civil and Environmental Engineering, Duke Global Health Institute, Duke University, Durham, North Carolina;
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Marc A. Deshusses
Marc A. Deshusses
Department of Civil and Environmental Engineering, Duke Global Health Institute, Duke University, Durham, North Carolina;
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Sachchida N. Tripathi
Sachchida N. Tripathi
Department of Civil Engineering, Centre for Environmental Science and Engineering, Indian Institute of Technology, Kanpur, India;
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Michael H. Bergin
Michael H. Bergin
Department of Civil and Environmental Engineering, Duke Global Health Institute, Duke University, Durham, North Carolina;
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Joe Brown
Joe Brown
Deparment of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, North Carolina
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ABSTRACT
Understanding the movement of antimicrobial resistance genes (ARGs) in the environment is critical to managing their spread. To assess potential ARG transport through the air via urban bioaerosols in cities with poor sanitation, we quantified ARGs and a mobile integron (MI) in ambient air over periods spanning rainy and dry seasons in Kanpur, India (n = 53), where open wastewater canals (OWCs) are prevalent. Gene targets represented major antibiotic groups—tetracyclines (tetA), fluoroquinolines (qnrB), and beta-lactams (blaTEM)—and a class 1 mobile integron (intI1). Over half of air samples located near, and up to 1 km from OWCs with fecal contamination (n = 45) in Kanpur had detectable targets above the experimentally determined limits of detection (LOD): most commonly intI1 and tetA (56% and 51% of samples, respectively), followed by blaTEM (8.9%) and qnrB (0%). ARG and MI densities in these positive air samples ranged from 6.9 × 101 to 5.2 × 103 gene copies/m3 air. Most (7/8) control samples collected 1 km away from OWCs were negative for any targets. In comparing experimental samples with control samples, we found that intI1 and tetA densities in air are significantly higher (P = 0.04 and P = 0.01, respectively, alpha = 0.05) near laboratory-confirmed fecal contaminated waters than at the control site. These data suggest increased densities of ARGs and MIs in bioaerosols in urban environments with inadequate sanitation. In such settings, aerosols may play a role in the spread of AR.
- Supplemental Materials (DOCX 75.40 KB)
Author Notes
Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the CDC.
Financial support: This material is based on work supported by the National Science Foundation under grant number 1653226.
Authors’ addresses: Olivia Ginn, School of Civil and Environmental Engineering, Georgia Institute of Technology, Atlanta, GA, E-mail: ginnolivia@gmail.com. David Berendes, Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Diseases, Centers for Disease Control and Prevention, Atlanta, GA, E-mail: uws8@cdc.gov. Anna Wood, Department of Epidemiology, Rollins School of Public Health, Emory University, Atlanta, GA, E-mail: anna.wood@emory.edu. Aaron Bivins, Department of Civil and Environmental Engineering and Earth Science, University of Notre Dame, Notre Dame, IN, E-mail: abivins@nd.edu. Lucas Rocha-Melogno, Marc A. Deshusses, and Mike Bergin, Department of Civil and Environmental Engineering, and Duke Global Health Institute, Duke University, Durham, NC, E-mails: lucas.rocha.melogno@duke.edu, marc.deshusses@duke.edu, and michael.bergin@duke.edu. Joe Brown, Deparment of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, E-mail: joebrown@unc.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Vikesland PJ et al. 2017. Toward a comprehensive strategy to mitigate dissemination of environmental sources of antibiotic resistance. Environ Sci Technol 51: 13061–13069.
-
2.
de J, Sosal A, Byarugaba DK, Amabile-Cuevas CF, Hsueh PR, Kariuki S, Okeke IN, eds. 2010. Antimicrobial Resistance in Developing Countries Berling/Heidelberg, Germany: Springer Science and Buisiness Media, 3–36. doi: 10.1007/s13312-014-0374-3.
-
3.
Davies J, Davies D, 2010. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74: 417–433.
-
4.
Pruden A, Pei R, Storteboom H, Carlson KH, 2006. Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 40: 7445–7450.
-
5.
GARP, 2011. Rationalizing antibiotic use to limit antibiotic resistance in India. Indian J Med Res 134: 3193708.
-
6.
Laxminarayan R, Chaudhuryanan RR, 2016. Antibiotic resistance in India: drivers and opportunities for action. PLoS Med 13: e1001974. doi: 10.1371/journal.pmed.1001974.
-
7.
Shahid M, Singh A, Sobia F, Rashid M, Malik A, Shukla I, Khan HM, 2011. Bla CTX-M, bla TEM, and bla SHV in Enterobacteriaceae from North-Indian tertiary hospital: high occurrence of combination genes. Asian Pac J Trop Med 4: 101–105.
-
8.
Prakash S, 2006. Carbapenem sensitivity profile amongst bacterial isolates from clinical specimens in Kanpur city. Indian J Crit Care Med 10: 10–13.
-
9.
Bennett PM, 2008. Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 153: 347–357.
-
10.
Schrag SJ, McGee L, Whitney CG, Beall B, Craig AS, Choate ME, Jorgensen JH, Facklam RR, Klugman KP, 2004. Emergence of Streptococcus pneumoniae with very-high-level resistance to penicillin. Antimicrob Agents Chemother 48: 3016–3023.
-
11.
Wellington EMH et al. 2013. The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect Dis 13: 155–165.
-
12.
Gao X, Shao M, Luo Y, Dong Y, Ouyang F, Dong W, Li J, 2016. Airborne bacterial contaminations in typical Chinese wet market with live poultry trade. Sci Total Environ 572: 681–687.
-
13.
Li J, Zhou L, Zhang X, Xu C, Dong L, Yao M, 2016. Bioaerosol emissions and detection of airborne antibiotic resistance genes from a wastewater treatment plant. Atmos Environ 124: 404–412.
-
14.
Echeverria-Palencia CM et al. 2017. Disparate antibiotic resistance gene quantities revealed across 4 major cities in California: a survey in drinking water, air, and soil at 24 public parks. ACS Omega 2: 2255–2263.
-
15.
Sancheza HM et al. 2016. Antibiotic resistance in airborne bacteria near conventional and organic beef cattle farms in California, USA. Water Air Soil Pollut: 227–280. doi: 10.1007/s11270-016-2979-8.
-
16.
Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D, 2013. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447: 345–360.
-
17.
Liu D et al. 2012. Formation and transmission of Staphylococcus aureus (including MRSA) aerosols carrying antibiotic-resistant genes in a poultry farming environment. Sci Total Environ 426: 139–145.
-
18.
McEachran AD, Blackwell BR, Hanson JD, Wooten KJ, Mayer GD, Cox SB, Smith PN, 2015. Antibiotics, bacteria, and antibiotic resistance genes: aerial transport from cattle feed yards via particulate matter. Environ Health Perspect 123: 337–343.
-
19.
Hu J, Zhao F, Zhang XX, Li K, Li C, Ye L, Li M, 2018. Metagenomic profiling of ARGs in airborne particulate matters during a severe smog event. Sci Total Environ 615: 1332–1340.
-
20.
Li J et al. 2018. Global survey of antibiotic resistance genes in air. Environ Sci Technol 52: 10975–10984.
-
21.
Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM, 2013. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA 110: 3435–3440.
-
22.
Zhang M, Zuo J, Yu X, Shi X, Chen L, Li Z, 2017. Quantification of multi-antibiotic resistant opportunistic pathogenic bacteria in bioaerosols in and around a pharmaceutical wastewater treatment plant. J Environ Sci 72: 53–63.
-
23.
Witte W, 2000. Selective pressure by antibiotic use in livestock. Int J Antimicrob Agents 16: 19–24.
-
24.
Graham DW, Giesen MJ, Bunce JT, 2018. Strategic approach for prioritising local and regional sanitation interventions for reducing global antibiotic resistance. Water (Switzerland) 11: 27.
-
25.
Pehrsson EC et al. 2016. Interconnected microbiomes and resistomes in low-income human habitats. Nature 533: 212–216.
-
26.
Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DGJ, 2016. The structure and diversity of human, animal and environmental resistomes. Microbiome 4: 54.
-
27.
Gao M, Qiu T, Sun Y, Wang X, 2018. The abundance and diversity of antibiotic resistance genes in the atmospheric environment of composting plants. Environ Int 116: 229–238.
-
28.
Chapin A, Rule A, Gibson K, Buckley T, Schwab K, 2005. Airborne multidrug-resistant bacteria isolated from a concentrated swine feeding operation. Environ Health Perspect 113: 137–142.
-
29.
Gibbs SG, Green CF, Tarwater PM, Mota LC, Mena KD, Scarpino PV, 2006. Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environ Health Perspect 114: 1032–1037.
-
30.
Hyvärinen AP, Raatikainen T, Brus D, Komppula M, Panwar TS, Hooda RK, Sharma VP, Lihavainen H, 2011. Effect of the summer monsoon on aerosols at two measurement stations in Northern India–Part 1: PM and BC concentrations. Atmos Chem Phys 11: 8271–8282.
-
31.
Kumar P, 2011. Census of India, Series 10 Part XII–A District Census Handbook. Kanpur Nagar, Uttar Pradesh: Directorate of Census Operations.
-
32.
Singh RP, 2001. Effect of wastewater disposal and extent of industrial pollution in and around Kanpur, Uttar Pradesh, India. Bull Eng Geol Environ 60: 31–35.
-
33.
Zia H, Devadas V, 2008. Urban solid waste management in Kanpur: opportunities and perspectives. Habitat Int 32: 58–73.
-
34.
Murowchick P, Alburty D, 2013. Technical Report: Dry Filter Collection/Wet Elution Aspiration and Recovery Testing. Drexel, MO: AlburtyLab, Inc.
-
35.
Kodaka H, Mizuochi S, Teramura H, Nirazuka T, 2006. Comparison of the compact dry EC with the most probably number method (AOAC offical method 96624) for enumeration of Escherichia coli and coliform bacteria in raw meats. J AOAC Int 89: 100–114.
-
36.
Hill V, Narayanan J, Gallen R, Ferdinand K, Cromeans T, Vinjé J, 2015. Development of a nucleic acid extraction procedure for simultaneous recovery of DNA and RNA from diverse microbes in water. Pathogens 4: 335–354.
-
37.
Chiang C, Liu C, Weng L, Wang N, Liaw G, 2005. Presence of β -lactamase gene TEM-1 DNA sequence in commercial taq DNA polymerase. J Clin Microbiol 43: 530–532.
-
38.
Guarddon M, Miranda JM, Rodríguez JA, Vázquez BI, Cepeda A, Franco CM, 2011. Real-time polymerase chain reaction for the quantitative detection of tetA and tetB bacterial tetracycline resistance genes in food. Int J Food Microbiol 146: 284–289.
-
39.
Cavé L, Brothier E, Abrouk D, Bouda PS, Hien E, Nazaret S, 2016. Efficiency and sensitivity of the digital droplet PCR for the quantification of antibiotic resistance genes in soils and organic residues. Appl Microbiol Biotechnol 100: 10597–10608.
-
40.
Lachmayr KL, Cavanaugh CM, Kerkhof LJ, DiRienzo AG, Ford TE, 2009. Quantifying nonspecific tem β-lactamase (blatem) genes in a wastewater stream. Appl Environ Microbiol 75: 203–211.
-
41.
Barraud O, Baclet MC, Denis F, Ploy MC, 2010. Quantitative multiplex real-time PCR for detecting class 1, 2 and 3 integrons. J Antimicrob Chemother 65: 1642–1645.
-
42.
Holloway K, Mathai E, Sorensen T, Gray A, 2008. Community-based surveillance of antimicrobial use and resistance in resource-constrained settings. Anim Genet 39: 561–563.
-
43.
Stokdyk JP, Firnstahl AD, Spencer SK, Burch TR, Borchardt MA, 2016. Determining the 95% limit of detection for waterborne pathogen analyses from primary concentration to qPCR. Water Res 96: 105–113.
-
44.
Bivins A, Lowry S, Murphy HM, Borchardt M, Coyte R, Labhasetwar P, Brown J, 2020. Waterborne pathogen monitoring in Jaipur, India reveals potential microbial risks of urban groundwater supply. Npj Clean Water 3: 35.
-
45.
RC Team, 2018. A Language and Environment for Statistical Computing. Available at: https://www.r-project.org.
-
46.
Dueker ME, 2012. Connecting Water Quality with Air Quality Through Microbial Aerosols.
-
47.
Cronholm LS, 1980. Potential health hazards from microbial aerosols in densely populated urban regions. Appl Environ Microbiol 39: 6–12.
-
48.
Farling S, Rogers T, Knee JS, Tilley EA, Brown J, Deshusses MA, 2019. Bioaerosol emissions associated with pit latrine emptying operations. Sci Total Environ 648: 1082–1086.
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