Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance

Nicholas J. Ashbolt; Alejandro Amézquita; Thomas Backhaus; Peter Borriello; Kristian Koefoed Brandt; Peter Collignon; Anja Coors; Rita Finley; William H. Gaze; Thomas Heberer; John R. Lawrence; D.G. Joakim Larsson; Scott A. McEwen; James J. Ryan; Jens Schönfeld; Peter Silley; Jason R. Snape; Christel Van den Eede; Edward Topp

doi:10.1289/ehp.1206316

Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance

Nicholas J. Ashbolt, Alejandro Amézquita, Thomas Backhaus, Peter Borriello, Kristian Koefoed Brandt, Peter Collignon, Anja Coors, Rita Finley, William H. Gaze, Thomas Heberer, John R. Lawrence, D.G. Joakim Larsson, Scott A. McEwen, James J. Ryan, Jens Schönfeld, Peter Silley, Jason R. Snape, Christel Van den Eede, Edward Topp

Microbial Ecology and Biotechnology

320 Citations (Scopus)

Abstract

Background: Only recently has the environment been clearly implicated in the risk of antibiotic resistance to clinical outcome, but to date there have been few documented approaches to formally assess these risks. Objective: We examined possible approaches and sought to identify research needs to enable human health risk assessments (HHRA) that focus on the role of the environment in the failure of antibiotic treatment caused by antibiotic-resistant pathogens. Methods: The authors participated in a workshop held 4-8 March 2012 in Québec, Canada, to define the scope and objectives of an environmental assessment of antibiotic-resistance risks to human health. We focused on key elements of environmental-resistance-development "hot spots," exposure assessment (unrelated to food), and dose response to characterize risks that may improve antibiotic-resistance management options. Discussion: Various novel aspects to traditional risk assessments were identified to enable an assessment of environmental antibiotic resistance. These include a) accounting for an added selective pressure on the environmental resistome that, over time, allows for development of antibiotic-resistant bacteria (ARB); b) identifying and describing rates of horizontal gene transfer (HGT) in the relevant environmental "hot spot" compartments; and c) modifying traditional dose-response approaches to address doses of ARB for various health outcomes and pathways. Conclusions: We propose that environmental aspects of antibiotic-resistance development be included in the processes of any HHRA addressing ARB. Because of limited available data, a multi-criteria decision analysis approach would be a useful way to undertake an HHRA of environmental antibiotic resistance that informs risk managers.

Original language	English
Journal	Environmental Health Perspectives
Volume	121
Issue number	9
Pages (from-to)	993-1001
Number of pages	9
ISSN	0091-6765
DOIs	https://doi.org/10.1289/ehp.1206316
Publication status	Published - Sept 2013

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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. (2013). Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environmental Health Perspectives, 121(9), 993-1001. https://doi.org/10.1289/ehp.1206316

Ashbolt, NJ, Amézquita, A, Backhaus, T, Borriello, P, Brandt, KK, Collignon, P, Coors, A, Finley, R, Gaze, WH, Heberer, T, Lawrence, JR, Larsson, DGJ, McEwen, SA, Ryan, JJ, Schönfeld, J, Silley, P, Snape, JR, Van den Eede, C & Topp, E 2013, 'Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance', Environmental Health Perspectives, vol. 121, no. 9, pp. 993-1001. https://doi.org/10.1289/ehp.1206316

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abstract = "Background: Only recently has the environment been clearly implicated in the risk of antibiotic resistance to clinical outcome, but to date there have been few documented approaches to formally assess these risks. Objective: We examined possible approaches and sought to identify research needs to enable human health risk assessments (HHRA) that focus on the role of the environment in the failure of antibiotic treatment caused by antibiotic-resistant pathogens. Methods: The authors participated in a workshop held 4-8 March 2012 in Qu{\'e}bec, Canada, to define the scope and objectives of an environmental assessment of antibiotic-resistance risks to human health. We focused on key elements of environmental-resistance-development {"}hot spots,{"} exposure assessment (unrelated to food), and dose response to characterize risks that may improve antibiotic-resistance management options. Discussion: Various novel aspects to traditional risk assessments were identified to enable an assessment of environmental antibiotic resistance. These include a) accounting for an added selective pressure on the environmental resistome that, over time, allows for development of antibiotic-resistant bacteria (ARB); b) identifying and describing rates of horizontal gene transfer (HGT) in the relevant environmental {"}hot spot{"} compartments; and c) modifying traditional dose-response approaches to address doses of ARB for various health outcomes and pathways. Conclusions: We propose that environmental aspects of antibiotic-resistance development be included in the processes of any HHRA addressing ARB. Because of limited available data, a multi-criteria decision analysis approach would be a useful way to undertake an HHRA of environmental antibiotic resistance that informs risk managers.",

author = "Ashbolt, {Nicholas J.} and Alejandro Am{\'e}zquita and Thomas Backhaus and Peter Borriello and Brandt, {Kristian Koefoed} and Peter Collignon and Anja Coors and Rita Finley and Gaze, {William H.} and Thomas Heberer and Lawrence, {John R.} and Larsson, {D.G. Joakim} and McEwen, {Scott A.} and Ryan, {James J.} and Jens Sch{\"o}nfeld and Peter Silley and Snape, {Jason R.} and {Van den Eede}, Christel and Edward Topp",

year = "2013",

month = sep,

doi = "10.1289/ehp.1206316",

language = "English",

volume = "121",

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AU - Ashbolt, Nicholas J.

AU - Amézquita, Alejandro

AU - Backhaus, Thomas

AU - Borriello, Peter

AU - Brandt, Kristian Koefoed

AU - Collignon, Peter

AU - Coors, Anja

AU - Finley, Rita

AU - Gaze, William H.

AU - Heberer, Thomas

AU - Lawrence, John R.

AU - Larsson, D.G. Joakim

AU - McEwen, Scott A.

AU - Ryan, James J.

AU - Schönfeld, Jens

AU - Silley, Peter

AU - Snape, Jason R.

AU - Van den Eede, Christel

AU - Topp, Edward

PY - 2013/9

Y1 - 2013/9

N2 - Background: Only recently has the environment been clearly implicated in the risk of antibiotic resistance to clinical outcome, but to date there have been few documented approaches to formally assess these risks. Objective: We examined possible approaches and sought to identify research needs to enable human health risk assessments (HHRA) that focus on the role of the environment in the failure of antibiotic treatment caused by antibiotic-resistant pathogens. Methods: The authors participated in a workshop held 4-8 March 2012 in Québec, Canada, to define the scope and objectives of an environmental assessment of antibiotic-resistance risks to human health. We focused on key elements of environmental-resistance-development "hot spots," exposure assessment (unrelated to food), and dose response to characterize risks that may improve antibiotic-resistance management options. Discussion: Various novel aspects to traditional risk assessments were identified to enable an assessment of environmental antibiotic resistance. These include a) accounting for an added selective pressure on the environmental resistome that, over time, allows for development of antibiotic-resistant bacteria (ARB); b) identifying and describing rates of horizontal gene transfer (HGT) in the relevant environmental "hot spot" compartments; and c) modifying traditional dose-response approaches to address doses of ARB for various health outcomes and pathways. Conclusions: We propose that environmental aspects of antibiotic-resistance development be included in the processes of any HHRA addressing ARB. Because of limited available data, a multi-criteria decision analysis approach would be a useful way to undertake an HHRA of environmental antibiotic resistance that informs risk managers.

AB - Background: Only recently has the environment been clearly implicated in the risk of antibiotic resistance to clinical outcome, but to date there have been few documented approaches to formally assess these risks. Objective: We examined possible approaches and sought to identify research needs to enable human health risk assessments (HHRA) that focus on the role of the environment in the failure of antibiotic treatment caused by antibiotic-resistant pathogens. Methods: The authors participated in a workshop held 4-8 March 2012 in Québec, Canada, to define the scope and objectives of an environmental assessment of antibiotic-resistance risks to human health. We focused on key elements of environmental-resistance-development "hot spots," exposure assessment (unrelated to food), and dose response to characterize risks that may improve antibiotic-resistance management options. Discussion: Various novel aspects to traditional risk assessments were identified to enable an assessment of environmental antibiotic resistance. These include a) accounting for an added selective pressure on the environmental resistome that, over time, allows for development of antibiotic-resistant bacteria (ARB); b) identifying and describing rates of horizontal gene transfer (HGT) in the relevant environmental "hot spot" compartments; and c) modifying traditional dose-response approaches to address doses of ARB for various health outcomes and pathways. Conclusions: We propose that environmental aspects of antibiotic-resistance development be included in the processes of any HHRA addressing ARB. Because of limited available data, a multi-criteria decision analysis approach would be a useful way to undertake an HHRA of environmental antibiotic resistance that informs risk managers.

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EP - 1001

JO - Environmental Health Perspectives

JF - Environmental Health Perspectives

IS - 9

ER -

Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance

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