Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance
Type | Article | ||||||||||||||||||||||||||||||||
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Date | 2022-12 | ||||||||||||||||||||||||||||||||
Language | English | ||||||||||||||||||||||||||||||||
Author(s) | Munk Patrick1, Brinch Christian1, Duus Møller Frederik1, Petersen Thomas N.1, Hendriksen Rene S.1, Seyfarth Anne Mette1, Kjeldgaard Jette S.1, Svendsen Christina Aaby1, Van Bunnik Bram2, 3, Berglund Fanny3, Bego Artan5, Power Pablo6, Rees Catherine7, Lambrinidis Dionisia8, Neilson Elizabeth Heather Jakobsen9, Gibb Karen10, Coventry Kris7, Collignon Peter11, Cassar Susan12, Allerberger Franz13, Begum Anowara14, Hossain Zenat Zebin14, Worrell Carlon15, Vandenberg Olivier16, Pieters Ilse17, Victorien Dougnon Tamègnon18, Gutierrez Angela Daniela Salazar19, Soria Freddy19, Grujić Vesna Rudić20, Mazalica Nataša21, Rahube Teddie O.22, Tagliati Carlos Alberto23, Rodrigues Dalia24, Oliveira Guilherme25, de Souza Larissa Camila Ribeiro23, Ivanov Ivan26, Juste Bonkoungou Isidore27, Oumar Traoré27, Sopheak Thet28, Vuthy Yith28, Ngandijo Antoinette29, Nzouankeu Ariane29, Olivier Ziem A. Abah Jacques29, Yost Christopher K.30, Kumar Pratik31, Brar Satinder Kaur32, Tabo Djim-Adjim33, Adell Aiko D.34, Paredes-Osses Esteban35, Martinez Maria Cristina35, Cuadros-Orellana Sara36, Ke Changwen37, Zheng Huanying37, Baisheng Li37, Lau Lok Ting38, Chung Teresa38, Jiao Xiaoyang39, Yu Yongjie40, Jiayong Zhao41, Morales Johan F. Bernal42, Valencia Maria Fernanda42, Donado-Godoy Pilar42, Coulibaly Kalpy Julien43, Hrenovic Jasna44, Jergović Matijana45, Karpíšková Renáta46, Deogratias Zozo Nyarukweba47, Elsborg Bodil48, Hansen Lisbeth Truelstrup49, Jensen Pernille Erland49, Abouelnaga Mohamed50, Salem Mohamed Fathy51, Koolmeister Marliin52, Legesse Mengistu53, Eguale Tadesse53, Heikinheimo Annamari54, Le Guyader Soizick55, Schaeffer Julien55, Villacis Jose Eduardo56, Sanneh Bakary57, Malania Lile58, Nitsche Andreas59, Brinkmann Annika59, Schubert Sara60, Hesse Sina60, Berendonk Thomas U.60, Saba Courage Kosi Setsoafia61, Mohammed Jibril62, Feglo Patrick Kwame63, Banu Regina Ama64, Kotzamanidis Charalampos65, Lytras Efthymios66, Lickes Sergio A.67, Kocsis Bela68, Solymosi Norbert69, Thorsteinsdottir Thorunn R.70, Hatha Abdulla Mohamed71, Ballal Mamatha72, Bangera Sohan Rodney73, Fani Fereshteh74, Alebouyeh Masoud75, Morris Dearbhaile76, O’connor Louise76, Cormican Martin76, Moran-Gilad Jacob77, Battisti Antonio78, Diaconu Elena Lavinia78, Corno Gianluca79, Di Cesare Andrea79, Alba Patricia78, Hisatsune Junzo80, Yu Liansheng80, Kuroda Makoto80, Sugai Motoyuki80, Kayama Shizuo80, Shakenova Zeinegul81, Kiiyukia Ciira82, Ng’eno Eric83, Raka Lul84, Jamil Kazi85, Fakhraldeen Saja Adel85, Alaati Tareq85, Bērziņš Aivars86, Avsejenko Jeļena86, Kokina Kristina86, Streikisa Madara86, Bartkevics Vadims86, Matar Ghassan M.87, Daoud Ziad88, Pereckienė Asta89, Butrimaite-Ambrozeviciene Ceslova89, Penny Christian90, Bastaraud Alexandra91, Rasolofoarison Tiavina92, Collard Jean-Marc91, Samison Luc Hervé, Andrianarivelo Mala Rakoto92, Banda Daniel Lawadi93, Amin Arshana94, Rajandas Heraa95, Parimannan Sivachandran95, Spiteri David96, Haber Malcolm Vella97, Santchurn Sunita J.98, Vujacic Aleksandar99, Djurovic Dijana99, Bouchrif Brahim100, Karraouan Bouchra100, Vubil Delfino Carlos101, Pal Pushkar102, Schmitt Heike103, Van Passel Mark103, Jeunen Gert-Jan104, Gemmell Neil104, Chambers Stephen T.105, Mendoza Fania Perez106, Huete-Pιrez Jorge106, Vilchez Samuel107, Ahmed Akeem Olayiwola108, Adisa Ibrahim Raufu108, Odetokun Ismail Ayoade108, Fashae Kayode109, Sørgaard Anne-Marie110, Wester Astrid Louise110, Ryrfors Pia111, Holmstad Rune111, Mohsin Mashkoor112, Hasan Rumina113, Shakoor Sadia113, Gustafson Natalie Weiler114, Schill Claudia Huber114, Rojas Maria Luz Zamudio115, Velasquez Jorge Echevarria116, Magtibay Bonifacio B.117, Catangcatang Kris118, Sibulo Ruby118, Yauce Felipe Campos116, Wasyl Dariusz119, Manaia Celia120, Rocha Jaqueline120, Martins Jose121, Álvaro Pedro121, Di Yoong Wen Doris122, Shin Hanseob122, Hur Hor-Gil122, Yoon Sukhwan123, Bosevska Golubinka124, Kochubovski Mihail124, Cojocaru Radu125, Burduniuc Olga126, Hong Pei-Ying127, Perry Meghan Rose128, Gassama Amy129, Radosavljevic Vladimir130, Tay Moon Y. F.131, Zuniga-Montanez Rogelio131, Wuertz Stefan131, Gavačová Dagmar132, Pastuchová Katarína132, Truska Peter132, Trkov Marija133, Keddy Karen134, Esterhuyse Kerneels135, Song Min Joon136, Quintela-Baluja Marcos137, Lopez Mariano Gomez138, Cerdà-Cuéllar Marta139, Perera R. R. D. P.140, Bandara N. K. B. K. R. G. W.140, Premasiri H. I.140, Pathirage Sujatha141, Charlemagne Kareem142, Rutgersson Carolin143, Norrgren Leif144, Örn Stefan144, Boss Renate145, Van Der Heijden Tanja146, Hong Yu-Ping147, Kumburu Happiness Houka148, Mdegela Robinson Hammerthon149, Hounmanou Yaovi Mahuton Gildas9, Chonsin Kaknokrat150, Suthienkul Orasa151, Thamlikitkul Visanu152, de Roda Husman Ana Maria153, Bidjada Bawimodom154, Njanpop-Lafourcade Berthe-Marie155, Nikiema-Pessinaba Somtinda Christelle156, Levent Belkis157, Kurekci Cemil158, Ejobi Francis159, Kalule John Bosco159, Thomsen Jens160, Obaidi Ouidiane161, Jassim Laila Mohamed162, Moore Andrew163, Leonard Anne164, Graham David W.165, Bunce Joshua T.165, Zhang Lihong164, Gaze William H.164, Lefor Brett166, Capone Drew167, Sozzi Emanuele168, Brown Joe167, Meschke John Scott168, Sobsey Mark D.169, Davis Michael170, Beck Nicola Koren169, Sukapanpatharam Pardi169, Truong Phuong169, Lilienthal Ronald171, Kang Sanghoon172, Wittum Thomas E.173, Rigamonti Natalia174, Baklayan Patricia174, Van Chinh Dang175, Tran Doan Minh Nguyen175, Do Phuc Nguyen175, Kwenda Geoffrey176, Larsson D. G. Joakim3, Koopmans Marion4, Woolhouse Mark2, Aarestrup Frank M.1 | ||||||||||||||||||||||||||||||||
Affiliation(s) | 1 : Research Group for Genomic Epidemiology, Technical University of Denmark, Kgs, Lyngby, Denmark 2 : Centre for Immunity, Infection and Evolution, University of Edinburgh, Edinburgh, UK 3 : Centre for Antibiotic Resistance Research (CARe), University of Gothenburg, Gothenburg, Sweden 4 : Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands 5 : Institute of Public Health, Tirana, Albania 6 : Universidad de Buenos Aires, Buenos Aires, Argentina 7 : Melbourne Water Corporation, Melbourne, Australia 8 : Charles Darwin University, Darwin, Australia 9 : University of Copenhagen, Frederiksberg C, Denmark 10 : Charles Darwin University, Darwin Northern Territory, Australia 11 : Canberra Hospital, Canberra, Australia 12 : ALS Water, Scoresby, Australia 13 : Austrian Agency for Health and Food Safety (AGES), Vienna, Austria 14 : University of Dhaka, Dhaka, Bangladesh 15 : Environmental Protection Department, Bridgetown, St. Michael, Barbados 16 : Laboratoire Hospitalier Universitaire de Bruxelles (LHUB-ULB), Brussels, Belgium 17 : AQUAFIN NV, Aartselaar, Belgium 18 : Polytechnic School of Abomey-Calavi, Abomey-Calavi, Benin 19 : Universidad Catσlica Boliviana San Pablo, La Paz, Bolivia 20 : Public Health Institute of the Republic of Srpska, Faculty of Medicine University of Banja Luka, Banja Luka, Bosnia and Herzegovina 21 : Public Health Institute of the Republic of Srpska, Banja Luka, Bosnia and Herzegovina 22 : Botswana International University of Science and Technology, Palapye, Botswana 23 : Universidade Federal de Minas Gerais, Belo Horizonte, Brazil 24 : Oswaldo Cruz Institute, Rio de Janeiro, Brazil 25 : Vale Institute of Technology, Belιm, PA, Brazil 26 : National Center of Infectious and Parasitic Diseases, Sofia, Bulgaria 27 : University of Ouagadougou, Ouagadougou, Burkina Faso 28 : Institut Pasteur du Cambodge, Phnom Penh, Cambodia 29 : Centre Pasteur du Cameroun, Yaoundι, Cameroon 30 : University of Regina, Regina, Canada 31 : Eau Terre Environnement Research Centre (INRS-ETE), Quebec City G1K 9A9, Canada and Indian Institute of Technology, Jammu, India 32 : Eau Terre Environnement Research Centre (INRS-ETE), Quebec City G1K 9A9, Canada and Lassonde School of Enginerring, York University, Toronto, Canada 33 : University of N’Djamena, N’Djamena, Chad 34 : Escuela de Medicina Veterinaria, Facultad de Ciencias de la Vida, Universidad Andres Bello, Santiago, Chile 35 : Institute of Public Health, Santiago, Chile 36 : Centro de Biotecnologνa de los Recursos Naturales, Facultad de Ciencias Agrarias y Forestales, Talca, Chile 37 : Guangdong Provincial Center for Disease Control and Prevention, Guangzhou, China 38 : The Hong Kong Polytechnic University, Hong Kong, China 39 : Shantou University Medical College, Shantou, China 40 : Nanjing University of Information Science and Technology, Nanjing, China 41 : Center for Disease Control and Prevention of Henan province, Zhengzhou, China 42 : Colombian Integrated Program for Antimicrobial Resistance Surveillance - Coipars, CI Tibaitatα, Corporaciσn Colombiana de Investigaciσn Agropecuaria (AGROSAVIA), Tibaitatα - Mosquera, Cundinamarca, Colombia 43 : Institut Pasteur de Côte d’Ivoire, Abidjan, Côte d’Ivoire 44 : University of Zagreb, Zagreb, Croatia 45 : Andrija Stampar Teaching Institute of Public Health, Zagreb, Croatia 46 : Veterinary Research Institute, Brno, Czech Republic 47 : Centre de Recherche en Sciences Naturelles de Lwiro (CRSN-LWIRO), Bukavu, Democratic Republic of Congo 48 : BIOFOS A/S, Copenhagen K, Denmark 49 : Technical University of Denmark, Kgs., Lyngby, Denmark 50 : Suez Canal University, Ismailia, Egypt 51 : University of Sadat City, Sadat City, Egypt 52 : Ministry of Health, Environmental Microbiology, Tallinn, Estonia 53 : Addis Ababa University, Addis Ababa, Ethiopia 54 : University of Helsinki, Helsinki, Finland 55 : French Institute Search Pour L’exploitation De La Mer (Ifremer), Nantes, France 56 : Instituto Nacional de Investigaciσn en Salud Pϊblica-INSPI (CRNRAM), Galαpagos, Quito, Ecuador 57 : National Public Health Laboratories, Ministry of Health and Social Welfare, Kotu, Gambia 58 : National Center for Disease Control and Public Health, Tbilisi, Georgia 59 : Robert Koch Institute, Berlin, Germany 60 : Technische Universitδt Dresden, Institute of Hydrobiology, Dresden, Germany 61 : University for Development Studies, Tamale, Ghana 62 : University of Ghana, Accra, Ghana 63 : Kwame Nkrumah University of Science and Technology, Kumasi, PMB, Ghana 64 : Council for Scientific and Industrial Research Water Research Institute, Accra, Ghana 65 : Veterinary Research Institute of Thessaloniki, Hellenic Agricultural Organisation-DEMETER, Thermi, Greece 66 : Athens Water Supply and Sewerage Company (EYDAP S.A.), Athens, Greece 67 : Universidad de San Carlos de Guatemala, Guatemala City, Guatemala 68 : Semmelweis University, Institute of Medical Microbiology, Budapest, Hungary 69 : University of Veterinary Medicine, Budapest, Hungary 70 : University of Iceland, Reykjavνk, Iceland 71 : Cochin University of Science and Technology, Cochin, India 72 : Kasturba Medical College, Manipal, India 73 : Apollo Diagnostics, Mangalore, India 74 : Shiraz University of Medical Sciences, Shiraz, Iran 75 : Shahid Beheshti University of Medical Sciences, Tehran, Iran 76 : National University of Ireland Galway, Galway, Ireland 77 : Ben Gurion University of the Negev and Ministry of Health, Beer-Sheva, Israel 78 : Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Rome, Italy 79 : CNR - Water Research Institute, Verbania, Italy 80 : National Institute of Infectious Diseases, Tokyo, Japan 81 : National Center of Expertise, Taldykorgan, Kazakhstan 82 : Mount Kenya University, Thika, Kenya 83 : Kenya Medical Research Institute, Nairobi, Kenya 84 : University of Prishtina “Hasan Prishtina” & National Institute of Public Health of Kosovo, Pristina, Kosovo 85 : Kuwait Institute for Scientific Research, Kuwait City, Kuwait 86 : Institute of Food Safety, Riga, Latvia 87 : American University of Beirut, Beirut, Lebanon 88 : Central Michigan University & Michigan Health Clinics, Saginaw, MI, USA 89 : National Food and Veterinary Risk Assessment Institute, Vilnius, Lithuania 90 : Luxembourg Institute of Science and Technology, Belvaux, Luxembourg 91 : Institut Pasteur de Madagascar, Antananarivo, Madagascar 92 : University of Antananarivo, Centre d’Infectiologie Charles Mιrieux, Antananarivo, Madagascar 93 : University of Malawi, Blantyre, Malawi 94 : Malaysian Genomics Resource Centre Berhad, Kuala Lumpur, Malaysia 95 : AIMST University, COMBio, Kedah, Malaysia 96 : Water Services Corporation, Luqa, Malta 97 : Environmental Health Directorate, St. Venera, Malta 98 : University of Mauritius, Reduit, Mauritius 99 : Institute for Public Health Montenegro, Podgorica, Montenegro 100 : Institut Pasteur du Maroc, Casablanca, Morocco 101 : Centro de Investigaηγo em Saϊde de Manhiηa (CISM), Maputo, Mozambique 102 : Agriculture and Forestry University, Kathmandu, Nepal 103 : National Institute for Public, Health and the Environment (RIVM), Bilthoven, The Netherlands 104 : University of Otago, Dunedin, New Zealand 105 : University of Otago, Christchurch, New Zealand 106 : University of Central America, Managua, Nicaragua 107 : Universidad Nacional Autσnoma de Nicaragua-Leσn, Leσn, Nicaragua 108 : University of Ilorin, Ilorin, Nigeria 109 : University of Ibadan, Ibadan, Nigeria 110 : Norwegian Institute of Public Health, Oslo, Norway 111 : VEAS, Slemmestad, Norway 112 : University of Agriculture, Faisalabad, Pakistan 113 : Aga Khan University, Karachi, Pakistan 114 : Laboratorio Central de Salud Publica, Asuncion, Paraguay 115 : Instituto Nacional de Salud, Lima, Peru 116 : Universidad de Piura, Piura, Peru 117 : WHO Environmental and Occupational Health, Manila, Philippines 118 : Maynilad Water Services, Inc., Quezon City, Philippines 119 : National Veterinary Research Institute, Pulawy, Poland 120 : Universidade Catσlica Portuguesa, CBQF - Centro de Biotecnologia e Quνmica Fina - Laboratσrio Associado, Escola Superior de Biotecnologia, Porto, Portugal 121 : Aguas do Tejo Atlantico, Lisboa, Portugal 122 : Gwangju Institute of Science and Technology, Gwangju, Republic of Korea 123 : Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea 124 : institute of Public Health of the Republic of North Macedonia, Skopje, Republic of North Macedonia 125 : State Medical and Pharmaceutical University, Chișinău, Republic of Moldova 126 : National Agency for Public Health, Chișinău, Republic of Moldova 127 : King Abdullah University of Science and Technology, Thuwal, Saudi Arabia 128 : University of Edinburgh, Edinburgh, Scotland, UK 129 : Institut Pasteur de Dakar, Dakar, Senegal 130 : Institute of Veterinary Medicine of Serbia, Belgrade, Serbia 131 : Nanyang Technological University, Singapore, Singapore 132 : Public Health Authority of the Slovak Republic, Bratislava, Slovakia 133 : National Laboratory of Health, Environment and Food, Ljubljana, Slovenia 134 : Independent consultant, Johannesburg, South Africa 135 : Daspoort Waste Water Treatment Works, Pretoria, South Africa 136 : Korea Advanced Institute of Science and Technology, Daejeon, South Korea 137 : School of Veterinary Sciences, Lugo, Spain 138 : Labaqua, Santiago de Compostela, Spain 139 : IRTA, Centre de Recerca en Sanitat Animal (CReSA, IRTA-UAB), Campus de la Universitat Autonoma de Barcelona, Bellaterra, Spain 140 : University of Kelaniya, Ragama, Sri Lanka 141 : Medical Research Institute, Colombo, Sri Lanka 142 : Caribbean Public Health Agency, Catries, Saint Lucia 143 : The Sahlgrenska Academy at the University of Gothenburg, Gothenburg, Sweden 144 : Swedish University of Agricultural Sciences, Uppsala, Sweden 145 : Federal Food Safety and Veterinary Office (FSVO), Bern, Switzerland 146 : Ara Region Bern AG, Herrenschwanden, Switzerland 147 : Centers for Disease Control, Taipei, Taiwan 148 : Kilimanjaro Clinical Research Institute, Moshi, Tanzania 149 : Sokoine University of Agriculture, Morogoro, Tanzania 150 : Faculty of Science and Technology, Suratthani Rajabhat University, Surat Thani, Thailand 151 : Faculty of Public Health, Mahidol University, Bangkok, Thailand 152 : Faculty of Medicine Siriraj Hospital, Bangkok, Thailand 153 : National Institute for Public Health and the Environment (RIVM), Bilthoven, Netherlands 154 : National Institute of Hygiene, Lomι, Togo 155 : Agence de Médecine Préventive, Dapaong, Togo 156 : Division of Integrated Surveillance of Health Emergencies and Response, Lomι, Togo 157 : Public Health Institution of Turkey, Ankara, Turkey 158 : Hatay Mustafa Kemal University, Hatay, Turkey 159 : Makerere University, Kampala, Uganda 160 : Abu Dhabi Public Health Center, Abu Dhai, United Arab Emirates 161 : Dubai municipality, WWTP Al Aweer, Dubai, UAE 162 : Rashid Hospital, Dubai, UAE 163 : Northumbrian Water, Northumbria House, Abbey Road, Pity Me, Durham, UK 164 : University of Exeter Medical School, Cornwall, UK 165 : Newcastle University, Newcastle upon Tyne, UK 166 : Brightwater Treatment Plant, Woodinville, WA, USA 167 : Department of Environmental Sciences and Engineering, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA 168 : University of North Carolina, Chapel Hill, USA 169 : University of Washington, Seattle, WA, USA 170 : Baylor University, Waco, USA 171 : Columbia Boulevard WWTP, Portland, USA 172 : Eastern Illinois University, Charleston, USA 173 : The Ohio State University, Columbus Ohio, USA 174 : Laboratorio Tecnolσgico del Uruguay, Montevideo, Uruguay 175 : Institute of Public Health in Ho Chi Minh City, Ho Chi Minh, Vietnam 176 : University of Zambia, Lusaka, Zambia |
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Source | Nature Communications (2041-1723) (Springer Science and Business Media LLC), 2022-12 , Vol. 13 , N. 1 , P. 7251 (16p.) | ||||||||||||||||||||||||||||||||
DOI | 10.1038/s41467-022-34312-7 | ||||||||||||||||||||||||||||||||
WOS© Times Cited | 48 | ||||||||||||||||||||||||||||||||
Abstract | Antimicrobial resistance (AMR) is a major threat to global health. Understanding the emergence, evolution, and transmission of individual antibiotic resistance genes (ARGs) is essential to develop sustainable strategies combatting this threat. Here, we use metagenomic sequencing to analyse ARGs in 757 sewage samples from 243 cities in 101 countries, collected from 2016 to 2019. We find regional patterns in resistomes, and these differ between subsets corresponding to drug classes and are partly driven by taxonomic variation. The genetic environments of 49 common ARGs are highly diverse, with most common ARGs carried by multiple distinct genomic contexts globally and sometimes on plasmids. Analysis of flanking sequence revealed ARG-specific patterns of dispersal limitation and global transmission. Our data furthermore suggest certain geographies are more prone to transmission events and should receive additional attention. |
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