Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage

Rene S. Hendriksen; Patrick Munk; Patrick Njage; Bram van Bunnik; Luke McNally; Oksana Lukjancenko; Timo Röder; David Nieuwenhuijse; Susanne Karlsmose Pedersen; Jette Kjeldgaard; Rolf S. Kaas; Philip Thomas Lanken Conradsen Clausen; Josef Korbinian Vogt; Pimlapas Leekitcharoenphon; Milou G.M. van de Schans; Tina Zuidema; Ana Maria de Roda Husman; Simon Rasmussen; Bent Petersen; Artan Bego; Catherine Rees; Susan Cassar; Kris Coventry; Peter Collignon; Franz Allerberger; Teddie O. Rahube; Guilherme Oliveira; Ivan Ivanov; Yith Vuthy; Thet Sopheak; Christopher K. Yost; Changwen Ke; Huanying Zheng; Li Baisheng; Xiaoyang Jiao; Pilar Donado-Godoy; Kalpy Julien Coulibaly; Matijana Jergović; Jasna Hrenovic; Renáta Karpíšková; Jose Eduardo Villacis; Mengistu Legesse; Tadesse Eguale; Annamari Heikinheimo; Lile Malania; Andreas Nitsche; Annika Brinkmann; Courage Kosi Setsoafia Saba; Bela Kocsis; Norbert Solymosi; Thorunn R. Thorsteinsdottir; Abdulla Mohamed Hatha; Masoud Alebouyeh; Dearbhaile Morris; Martin Cormican; Louise O’Connor; Jacob Moran-Gilad; Patricia Alba; Antonio Battisti; Zeinegul Shakenova; Ciira Kiiyukia; Eric Ng’eno; Lul Raka; Jeļena Avsejenko; Aivars Bērziņš; Vadims Bartkevics; Christian Penny; Heraa Rajandas; Sivachandran Parimannan; Malcolm Vella Haber; Pushkar Pal; Gert Jan Jeunen; Neil Gemmell; Kayode Fashae; Rune Holmstad; Rumina Hasan; Sadia Shakoor; Maria Luz Zamudio Rojas; Dariusz Wasyl; Golubinka Bosevska; Mihail Kochubovski; Cojocaru Radu; Amy Gassama; Vladimir Radosavljevic; Stefan Wuertz; Rogelio Zuniga-Montanez; Moon Y.F. Tay; Dagmar Gavačová; Katarina Pastuchova; Peter Truska; Marija Trkov; Kerneels Esterhuyse; Karen Keddy; Marta Cerdà-Cuéllar; Sujatha Pathirage; Leif Norrgren; Stefan Örn; D. G.Joakim Larsson; Tanja Van der Heijden; Happiness Houka Kumburu; Bakary Sanneh; Pawou Bidjada; Berthe Marie Njanpop-Lafourcade; Somtinda Christelle Nikiema-Pessinaba; Belkis Levent; John Scott Meschke; Nicola Koren Beck; Chinh Dang Van; Nguyen Do Phuc; Doan Minh Nguyen Tran; Geoffrey Kwenda; Djim adjim Tabo; Astrid Louise Wester; Sara Cuadros-Orellana; Clara Amid; Guy Cochrane; Thomas Sicheritz-Ponten; Heike Schmitt; Jorge Raul Matheu Alvarez; Awa Aidara-Kane; Sünje J. Pamp; Ole Lund; Tine Hald; Mark Woolhouse; Marion P. Koopmans; Håkan Vigre; Thomas Nordahl Petersen; Frank M. Aarestrup

doi:10.1038/s41467-019-08853-3

Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage

Rene S. Hendriksen, Patrick Munk, Patrick Njage, Bram van Bunnik, Luke McNally, Oksana Lukjancenko, Timo Röder, David Nieuwenhuijse, Susanne Karlsmose Pedersen, Jette Kjeldgaard, Rolf S. Kaas, Philip Thomas Lanken Conradsen Clausen, Josef Korbinian Vogt, Pimlapas Leekitcharoenphon, Milou G.M. van de Schans, Tina Zuidema, Ana Maria de Roda Husman, Simon Rasmussen, Bent Petersen, Artan BegoCatherine Rees, Susan Cassar, Kris Coventry, Peter Collignon, Franz Allerberger, Teddie O. Rahube, Guilherme Oliveira, Ivan Ivanov, Yith Vuthy, Thet Sopheak, Christopher K. Yost, Changwen Ke, Huanying Zheng, Li Baisheng, Xiaoyang Jiao, Pilar Donado-Godoy, Kalpy Julien Coulibaly, Matijana Jergović, Jasna Hrenovic, Renáta Karpíšková, Jose Eduardo Villacis, Mengistu Legesse, Tadesse Eguale, Annamari Heikinheimo, Lile Malania, Andreas Nitsche, Annika Brinkmann, Courage Kosi Setsoafia Saba, Bela Kocsis, Norbert Solymosi, Thorunn R. Thorsteinsdottir, Abdulla Mohamed Hatha, Masoud Alebouyeh, Dearbhaile Morris, Martin Cormican, Louise O’Connor, Jacob Moran-Gilad, Patricia Alba, Antonio Battisti, Zeinegul Shakenova, Ciira Kiiyukia, Eric Ng’eno, Lul Raka, Jeļena Avsejenko, Aivars Bērziņš, Vadims Bartkevics, Christian Penny, Heraa Rajandas, Sivachandran Parimannan, Malcolm Vella Haber, Pushkar Pal, Gert Jan Jeunen, Neil Gemmell, Kayode Fashae, Rune Holmstad, Rumina Hasan, Sadia Shakoor, Maria Luz Zamudio Rojas, Dariusz Wasyl, Golubinka Bosevska, Mihail Kochubovski, Cojocaru Radu, Amy Gassama, Vladimir Radosavljevic, Stefan Wuertz, Rogelio Zuniga-Montanez, Moon Y.F. Tay, Dagmar Gavačová, Katarina Pastuchova, Peter Truska, Marija Trkov, Kerneels Esterhuyse, Karen Keddy, Marta Cerdà-Cuéllar, Sujatha Pathirage, Leif Norrgren, Stefan Örn, D. G.Joakim Larsson, Tanja Van der Heijden, Happiness Houka Kumburu, Bakary Sanneh, Pawou Bidjada, Berthe Marie Njanpop-Lafourcade, Somtinda Christelle Nikiema-Pessinaba, Belkis Levent, John Scott Meschke, Nicola Koren Beck, Chinh Dang Van, Nguyen Do Phuc, Doan Minh Nguyen Tran, Geoffrey Kwenda, Djim adjim Tabo, Astrid Louise Wester, Sara Cuadros-Orellana, Clara Amid, Guy Cochrane, Thomas Sicheritz-Ponten, Heike Schmitt, Jorge Raul Matheu Alvarez, Awa Aidara-Kane, Sünje J. Pamp, Ole Lund, Tine Hald, Mark Woolhouse, Marion P. Koopmans, Håkan Vigre, Thomas Nordahl Petersen, Frank M. Aarestrup

152 Citations (Scopus)

Abstract

Antimicrobial resistance (AMR) is a serious threat to global public health, but obtaining representative data on AMR for healthy human populations is difficult. Here, we use metagenomic analysis of untreated sewage to characterize the bacterial resistome from 79 sites in 60 countries. We find systematic differences in abundance and diversity of AMR genes between Europe/North-America/Oceania and Africa/Asia/South-America. Antimicrobial use data and bacterial taxonomy only explains a minor part of the AMR variation that we observe. We find no evidence for cross-selection between antimicrobial classes, or for effect of air travel between sites. However, AMR gene abundance strongly correlates with socio-economic, health and environmental factors, which we use to predict AMR gene abundances in all countries in the world. Our findings suggest that global AMR gene diversity and abundance vary by region, and that improving sanitation and health could potentially limit the global burden of AMR. We propose metagenomic analysis of sewage as an ethically acceptable and economically feasible approach for continuous global surveillance and prediction of AMR.

Original language	English
Article number	1124
Journal	Nature Communications
Volume	10
Issue number	1
Number of pages	12
ISSN	2041-1723
DOIs	https://doi.org/10.1038/s41467-019-08853-3
Publication status	Published - 1 Dec 2019
Externally published	Yes

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Global monitoring of antimicrobial resistance basedon metagenomics analyses of urban sewageFinal published version, 3.86 MB

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Hendriksen, R. S., Munk, P., Njage, P., van Bunnik, B., McNally, L., Lukjancenko, O., Röder, T., Nieuwenhuijse, D., Pedersen, S. K., Kjeldgaard, J., Kaas, R. S., Clausen, P. T. L. C., Vogt, J. K., Leekitcharoenphon, P., van de Schans, M. G. M., Zuidema, T., de Roda Husman, A. M., Rasmussen, S., Petersen, B., ... Aarestrup, F. M. (2019). Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. Nature Communications, 10(1), Article 1124. https://doi.org/10.1038/s41467-019-08853-3

Hendriksen, RS, Munk, P, Njage, P, van Bunnik, B, McNally, L, Lukjancenko, O, Röder, T, Nieuwenhuijse, D, Pedersen, SK, Kjeldgaard, J, Kaas, RS, Clausen, PTLC, Vogt, JK, Leekitcharoenphon, P, van de Schans, MGM, Zuidema, T, de Roda Husman, AM, Rasmussen, S , Petersen, B, Bego, A, Rees, C, Cassar, S, Coventry, K, Collignon, P, Allerberger, F, Rahube, TO, Oliveira, G, Ivanov, I, Vuthy, Y, Sopheak, T, Yost, CK, Ke, C, Zheng, H, Baisheng, L, Jiao, X, Donado-Godoy, P, Coulibaly, KJ, Jergović, M, Hrenovic, J, Karpíšková, R, Villacis, JE, Legesse, M, Eguale, T, Heikinheimo, A, Malania, L, Nitsche, A, Brinkmann, A, Saba, CKS, Kocsis, B, Solymosi, N, Thorsteinsdottir, TR, Hatha, AM, Alebouyeh, M, Morris, D, Cormican, M, O’Connor, L, Moran-Gilad, J, Alba, P, Battisti, A, Shakenova, Z, Kiiyukia, C, Ng’eno, E, Raka, L, Avsejenko, J, Bērziņš, A, Bartkevics, V, Penny, C, Rajandas, H, Parimannan, S, Haber, MV, Pal, P, Jeunen, GJ, Gemmell, N, Fashae, K, Holmstad, R, Hasan, R, Shakoor, S, Rojas, MLZ, Wasyl, D, Bosevska, G, Kochubovski, M, Radu, C, Gassama, A, Radosavljevic, V, Wuertz, S, Zuniga-Montanez, R, Tay, MYF, Gavačová, D, Pastuchova, K, Truska, P, Trkov, M, Esterhuyse, K, Keddy, K, Cerdà-Cuéllar, M, Pathirage, S, Norrgren, L, Örn, S, Larsson, DGJ, Heijden, TVD, Kumburu, HH, Sanneh, B, Bidjada, P, Njanpop-Lafourcade, BM, Nikiema-Pessinaba, SC, Levent, B, Meschke, JS, Beck, NK, Van, CD, Phuc, ND, Tran, DMN, Kwenda, G, Tabo, DA, Wester, AL, Cuadros-Orellana, S, Amid, C, Cochrane, G, Sicheritz-Ponten, T, Schmitt, H, Alvarez, JRM, Aidara-Kane, A, Pamp, SJ, Lund, O, Hald, T, Woolhouse, M, Koopmans, MP, Vigre, H, Petersen, TN & Aarestrup, FM 2019, 'Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage', Nature Communications, vol. 10, no. 1, 1124. https://doi.org/10.1038/s41467-019-08853-3

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title = "Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage",

abstract = "Antimicrobial resistance (AMR) is a serious threat to global public health, but obtaining representative data on AMR for healthy human populations is difficult. Here, we use metagenomic analysis of untreated sewage to characterize the bacterial resistome from 79 sites in 60 countries. We find systematic differences in abundance and diversity of AMR genes between Europe/North-America/Oceania and Africa/Asia/South-America. Antimicrobial use data and bacterial taxonomy only explains a minor part of the AMR variation that we observe. We find no evidence for cross-selection between antimicrobial classes, or for effect of air travel between sites. However, AMR gene abundance strongly correlates with socio-economic, health and environmental factors, which we use to predict AMR gene abundances in all countries in the world. Our findings suggest that global AMR gene diversity and abundance vary by region, and that improving sanitation and health could potentially limit the global burden of AMR. We propose metagenomic analysis of sewage as an ethically acceptable and economically feasible approach for continuous global surveillance and prediction of AMR.",

author = "Hendriksen, {Rene S.} and Patrick Munk and Patrick Njage and {van Bunnik}, Bram and Luke McNally and Oksana Lukjancenko and Timo R{\"o}der and David Nieuwenhuijse and Pedersen, {Susanne Karlsmose} and Jette Kjeldgaard and Kaas, {Rolf S.} and Clausen, {Philip Thomas Lanken Conradsen} and Vogt, {Josef Korbinian} and Pimlapas Leekitcharoenphon and {van de Schans}, {Milou G.M.} and Tina Zuidema and {de Roda Husman}, {Ana Maria} and Simon Rasmussen and Bent Petersen and Artan Bego and Catherine Rees and Susan Cassar and Kris Coventry and Peter Collignon and Franz Allerberger and Rahube, {Teddie O.} and Guilherme Oliveira and Ivan Ivanov and Yith Vuthy and Thet Sopheak and Yost, {Christopher K.} and Changwen Ke and Huanying Zheng and Li Baisheng and Xiaoyang Jiao and Pilar Donado-Godoy and Coulibaly, {Kalpy Julien} and Matijana Jergovi{\'c} and Jasna Hrenovic and Ren{\'a}ta Karp{\'i}{\v s}kov{\'a} and Villacis, {Jose Eduardo} and Mengistu Legesse and Tadesse Eguale and Annamari Heikinheimo and Lile Malania and Andreas Nitsche and Annika Brinkmann and Saba, {Courage Kosi Setsoafia} and Bela Kocsis and Norbert Solymosi and Thorsteinsdottir, {Thorunn R.} and Hatha, {Abdulla Mohamed} and Masoud Alebouyeh and Dearbhaile Morris and Martin Cormican and Louise O{\textquoteright}Connor and Jacob Moran-Gilad and Patricia Alba and Antonio Battisti and Zeinegul Shakenova and Ciira Kiiyukia and Eric Ng{\textquoteright}eno and Lul Raka and Jeļena Avsejenko and Aivars Bērziņ{\v s} and Vadims Bartkevics and Christian Penny and Heraa Rajandas and Sivachandran Parimannan and Haber, {Malcolm Vella} and Pushkar Pal and Jeunen, {Gert Jan} and Neil Gemmell and Kayode Fashae and Rune Holmstad and Rumina Hasan and Sadia Shakoor and Rojas, {Maria Luz Zamudio} and Dariusz Wasyl and Golubinka Bosevska and Mihail Kochubovski and Cojocaru Radu and Amy Gassama and Vladimir Radosavljevic and Stefan Wuertz and Rogelio Zuniga-Montanez and Tay, {Moon Y.F.} and Dagmar Gava{\v c}ov{\'a} and Katarina Pastuchova and Peter Truska and Marija Trkov and Kerneels Esterhuyse and Karen Keddy and Marta Cerd{\`a}-Cu{\'e}llar and Sujatha Pathirage and Leif Norrgren and Stefan {\"O}rn and Larsson, {D. G.Joakim} and Heijden, {Tanja Van der} and Kumburu, {Happiness Houka} and Bakary Sanneh and Pawou Bidjada and Njanpop-Lafourcade, {Berthe Marie} and Nikiema-Pessinaba, {Somtinda Christelle} and Belkis Levent and Meschke, {John Scott} and Beck, {Nicola Koren} and Van, {Chinh Dang} and Phuc, {Nguyen Do} and Tran, {Doan Minh Nguyen} and Geoffrey Kwenda and Tabo, {Djim adjim} and Wester, {Astrid Louise} and Sara Cuadros-Orellana and Clara Amid and Guy Cochrane and Thomas Sicheritz-Ponten and Heike Schmitt and Alvarez, {Jorge Raul Matheu} and Awa Aidara-Kane and Pamp, {S{\"u}nje J.} and Ole Lund and Tine Hald and Mark Woolhouse and Koopmans, {Marion P.} and H{\aa}kan Vigre and Petersen, {Thomas Nordahl} and Aarestrup, {Frank M.}",

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doi = "10.1038/s41467-019-08853-3",

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T1 - Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage

AU - Hendriksen, Rene S.

AU - Munk, Patrick

AU - Njage, Patrick

AU - van Bunnik, Bram

AU - McNally, Luke

AU - Lukjancenko, Oksana

AU - Röder, Timo

AU - Nieuwenhuijse, David

AU - Pedersen, Susanne Karlsmose

AU - Kjeldgaard, Jette

AU - Kaas, Rolf S.

AU - Clausen, Philip Thomas Lanken Conradsen

AU - Vogt, Josef Korbinian

AU - Leekitcharoenphon, Pimlapas

AU - van de Schans, Milou G.M.

AU - Zuidema, Tina

AU - de Roda Husman, Ana Maria

AU - Rasmussen, Simon

AU - Petersen, Bent

AU - Bego, Artan

AU - Rees, Catherine

AU - Cassar, Susan

AU - Coventry, Kris

AU - Collignon, Peter

AU - Allerberger, Franz

AU - Rahube, Teddie O.

AU - Oliveira, Guilherme

AU - Ivanov, Ivan

AU - Vuthy, Yith

AU - Sopheak, Thet

AU - Yost, Christopher K.

AU - Ke, Changwen

AU - Zheng, Huanying

AU - Baisheng, Li

AU - Jiao, Xiaoyang

AU - Donado-Godoy, Pilar

AU - Coulibaly, Kalpy Julien

AU - Jergović, Matijana

AU - Hrenovic, Jasna

AU - Karpíšková, Renáta

AU - Villacis, Jose Eduardo

AU - Legesse, Mengistu

AU - Eguale, Tadesse

AU - Heikinheimo, Annamari

AU - Malania, Lile

AU - Nitsche, Andreas

AU - Brinkmann, Annika

AU - Saba, Courage Kosi Setsoafia

AU - Kocsis, Bela

AU - Solymosi, Norbert

AU - Thorsteinsdottir, Thorunn R.

AU - Hatha, Abdulla Mohamed

AU - Alebouyeh, Masoud

AU - Morris, Dearbhaile

AU - Cormican, Martin

AU - O’Connor, Louise

AU - Moran-Gilad, Jacob

AU - Alba, Patricia

AU - Battisti, Antonio

AU - Shakenova, Zeinegul

AU - Kiiyukia, Ciira

AU - Ng’eno, Eric

AU - Raka, Lul

AU - Avsejenko, Jeļena

AU - Bērziņš, Aivars

AU - Bartkevics, Vadims

AU - Penny, Christian

AU - Rajandas, Heraa

AU - Parimannan, Sivachandran

AU - Haber, Malcolm Vella

AU - Pal, Pushkar

AU - Jeunen, Gert Jan

AU - Gemmell, Neil

AU - Fashae, Kayode

AU - Holmstad, Rune

AU - Hasan, Rumina

AU - Shakoor, Sadia

AU - Rojas, Maria Luz Zamudio

AU - Wasyl, Dariusz

AU - Bosevska, Golubinka

AU - Kochubovski, Mihail

AU - Radu, Cojocaru

AU - Gassama, Amy

AU - Radosavljevic, Vladimir

AU - Wuertz, Stefan

AU - Zuniga-Montanez, Rogelio

AU - Tay, Moon Y.F.

AU - Gavačová, Dagmar

AU - Pastuchova, Katarina

AU - Truska, Peter

AU - Trkov, Marija

AU - Esterhuyse, Kerneels

AU - Keddy, Karen

AU - Cerdà-Cuéllar, Marta

AU - Pathirage, Sujatha

AU - Norrgren, Leif

AU - Örn, Stefan

AU - Larsson, D. G.Joakim

AU - Heijden, Tanja Van der

AU - Kumburu, Happiness Houka

AU - Sanneh, Bakary

AU - Bidjada, Pawou

AU - Njanpop-Lafourcade, Berthe Marie

AU - Nikiema-Pessinaba, Somtinda Christelle

AU - Levent, Belkis

AU - Meschke, John Scott

AU - Beck, Nicola Koren

AU - Van, Chinh Dang

AU - Phuc, Nguyen Do

AU - Tran, Doan Minh Nguyen

AU - Kwenda, Geoffrey

AU - Tabo, Djim adjim

AU - Wester, Astrid Louise

AU - Cuadros-Orellana, Sara

AU - Amid, Clara

AU - Cochrane, Guy

AU - Sicheritz-Ponten, Thomas

AU - Schmitt, Heike

AU - Alvarez, Jorge Raul Matheu

AU - Aidara-Kane, Awa

AU - Pamp, Sünje J.

AU - Lund, Ole

AU - Hald, Tine

AU - Woolhouse, Mark

AU - Koopmans, Marion P.

AU - Vigre, Håkan

AU - Petersen, Thomas Nordahl

AU - Aarestrup, Frank M.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Antimicrobial resistance (AMR) is a serious threat to global public health, but obtaining representative data on AMR for healthy human populations is difficult. Here, we use metagenomic analysis of untreated sewage to characterize the bacterial resistome from 79 sites in 60 countries. We find systematic differences in abundance and diversity of AMR genes between Europe/North-America/Oceania and Africa/Asia/South-America. Antimicrobial use data and bacterial taxonomy only explains a minor part of the AMR variation that we observe. We find no evidence for cross-selection between antimicrobial classes, or for effect of air travel between sites. However, AMR gene abundance strongly correlates with socio-economic, health and environmental factors, which we use to predict AMR gene abundances in all countries in the world. Our findings suggest that global AMR gene diversity and abundance vary by region, and that improving sanitation and health could potentially limit the global burden of AMR. We propose metagenomic analysis of sewage as an ethically acceptable and economically feasible approach for continuous global surveillance and prediction of AMR.

AB - Antimicrobial resistance (AMR) is a serious threat to global public health, but obtaining representative data on AMR for healthy human populations is difficult. Here, we use metagenomic analysis of untreated sewage to characterize the bacterial resistome from 79 sites in 60 countries. We find systematic differences in abundance and diversity of AMR genes between Europe/North-America/Oceania and Africa/Asia/South-America. Antimicrobial use data and bacterial taxonomy only explains a minor part of the AMR variation that we observe. We find no evidence for cross-selection between antimicrobial classes, or for effect of air travel between sites. However, AMR gene abundance strongly correlates with socio-economic, health and environmental factors, which we use to predict AMR gene abundances in all countries in the world. Our findings suggest that global AMR gene diversity and abundance vary by region, and that improving sanitation and health could potentially limit the global burden of AMR. We propose metagenomic analysis of sewage as an ethically acceptable and economically feasible approach for continuous global surveillance and prediction of AMR.

U2 - 10.1038/s41467-019-08853-3

DO - 10.1038/s41467-019-08853-3

M3 - Journal article

C2 - 30850636

SN - 2041-1723

VL - 10

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 1124

ER -

Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage

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