Multiancestry association study identifies new asthma risk loci that colocalize with immune-cell enhancer marks.,Nature Genetics

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Multiancestry association study identifies new asthma risk loci that colocalize with immune-cell enhancer marks.
Nature Genetics ( IF 30.8 ) Pub Date : 2018-Jan-01 , DOI: 10.1038/s41588-017-0014-7
Florence Demenais _{1,

2} , Patricia Margaritte-Jeannin _{1,

2} , Kathleen C Barnes ₃ , William O C Cookson ₄ , Janine Altmüller ₅ , Wei Ang ₆ , R Graham Barr ₇ , Terri H Beaty ₈ , Allan B Becker ₉ , John Beilby ₁₀ , Hans Bisgaard ₁₁ , Unnur Steina Bjornsdottir ₁₂ , Eugene Bleecker ₁₃ , Klaus Bønnelykke ₁₁ , Dorret I Boomsma ₁₄ , Emmanuelle Bouzigon _{1,

2} , Christopher E Brightling ₁₅ , Myriam Brossard _{1,

2} , Guy G Brusselle _{16,

17,

18} , Esteban Burchard ₁₉ , Kristin M Burkart ₂₀ , Andrew Bush _{21,

22} , Moira Chan-Yeung ₂₃ , Kian Fan Chung _{21,

24} , Alexessander Couto Alves ₂₅ , John A Curtin ₂₆ , Adnan Custovic ₂₇ , Denise Daley _{23,

28} , Johan C de Jongste ₂₉ , Blanca E Del-Rio-Navarro ₃₀ , Kathleen M Donohue ₇ , Liesbeth Duijts ₃₁ , Celeste Eng ₃₂ , Johan G Eriksson ₃₃ , Martin Farrall _{34,

35} , Yuliya Fedorova ₃₆ , Bjarke Feenstra ₃₇ , Manuel A Ferreira ₃₈ , , Maxim B Freidin ₃₉ , Zofia Gajdos _{40,

41} , Jim Gauderman ₄₂ , Ulrike Gehring ₄₃ , Frank Geller ₃₇ , Jon Genuneit ₄₄ , Sina A Gharib ₄₅ , Frank Gilliland ₄₂ , Raquel Granell _{46,

47} , Penelope E Graves ₄₈ , Daniel F Gudbjartsson _{49,

50} , Tari Haahtela ₅₁ , Susan R Heckbert ₅₂ , Dick Heederik ₄₃ , Joachim Heinrich _{53,

54} , Markku Heliövaara ₅₅ , John Henderson _{46,

47} , Blanca E Himes ₅₆ , Hiroshi Hirose ₅₇ , Joel N Hirschhorn _{41,

58,

59} , Albert Hofman _{17,

60} , Patrick Holt ₆₁ , Jouke Hottenga ₁₄ , Thomas J Hudson _{62,

63} , Jennie Hui _{10,

64,

65} , Medea Imboden _{66,

67} , Vladimir Ivanov ₆₈ , Vincent W V Jaddoe ₆₉ , Alan James _{70,

71} , Christer Janson ₇₂ , Marjo-Riitta Jarvelin _{73,

74,

75,

76} , Deborah Jarvis _{21,

77} , Graham Jones ₇₈ , Ingileif Jonsdottir _{49,

79} , Pekka Jousilahti ₅₅ , Michael Kabesch ₈₀ , Mika Kähönen ₈₁ , David B Kantor _{82,

83} , Alexandra S Karunas _{36,

84} , Elza Khusnutdinova _{36,

84} , Gerard H Koppelman _{85,

86} , Anita L Kozyrskyj ₈₇ , Eskil Kreiner ₁₁ , Michiaki Kubo ₈₈ , Rajesh Kumar _{89,

90} , Ashish Kumar _{66,

67,

91} , Mikko Kuokkanen _{55,

92} , Lies Lahousse _{17,

93} , Tarja Laitinen ₉₄ , Catherine Laprise _{95,

96} , Mark Lathrop ₉₇ , Susanne Lau ₉₈ , Young-Ae Lee _{99,

100} , Terho Lehtimäki ₁₀₁ , Sébastien Letort _{1,

2} , Albert M Levin ₁₀₂ , Guo Li ₄₅ , Liming Liang _{60,

103} , Laura R Loehr ₁₀₄ , Stephanie J London ₁₀₅ , Daan W Loth ₁₇ , Ani Manichaikul ₁₀₆ , Ingo Marenholz _{99,

100} , Fernando J Martinez ₄₈ , Melanie C Matheson ₁₀₇ , Rasika A Mathias ₁₀₈ , Kenji Matsumoto ₁₀₉ , Hamdi Mbarek ₁₄ , Wendy L McArdle ₁₁₀ , Mads Melbye _{37,

111,

112} , Erik Melén _{91,

113,

114} , Deborah Meyers ₁₃ , Sven Michel ₈₀ , Hamida Mohamdi _{1,

2} , Arthur W Musk _{115,

116} , Rachel A Myers ₁₁₇ , Maartje A E Nieuwenhuis _{86,

118} , Emiko Noguchi ₁₁₉ , George T O'Connor _{120,

121} , Ludmila M Ogorodova ₁₂₂ , Cameron D Palmer _{41,

58} , Aarno Palotie _{92,

123,

124} , Julie E Park ₂₃ , Craig E Pennell ₆ , Göran Pershagen _{91,

113} , Alexey Polonikov ₆₈ , Dirkje S Postma _{86,

118} , Nicole Probst-Hensch _{66,

67} , Valery P Puzyrev ₃₉ , Benjamin A Raby ₁₂₅ , Olli T Raitakari ₁₂₆ , Adaikalavan Ramasamy _{25,

127} , Stephen S Rich ₁₀₆ , Colin F Robertson ₁₂₈ , Isabelle Romieu _{129,

130} , Muhammad T Salam _{42,

131} , Veikko Salomaa ₅₅ , Vivi Schlünssen ₁₃₂ , Robert Scott ₁₃₃ , Polina A Selivanova ₁₃₄ , Torben Sigsgaard ₁₃₂ , Angela Simpson _{26,

135} , Valérie Siroux _{136,

137} , Lewis J Smith ₁₃₈ , Maria Solodilova ₆₈ , Marie Standl ₅₄ , Kari Stefansson _{49,

79} , David P Strachan ₁₃₉ , Bruno H Stricker _{17,

140,

141} , Atsushi Takahashi ₈₈ , Philip J Thompson ₁₄₂ , Gudmar Thorleifsson ₄₉ , Unnur Thorsteinsdottir _{49,

79} , Carla M T Tiesler _{54,

143} , Dara G Torgerson ₃₂ , Tatsuhiko Tsunoda _{88,

144} , André G Uitterlinden ₁₄₁ , Ralf J P van der Valk ₁₄₅ , Amaury Vaysse _{1,

2} , Sailaja Vedantam _{40,

41} , Andrea von Berg ₁₄₆ , Erika von Mutius _{147,

148} , Judith M Vonk _{86,

149} , Johannes Waage ₁₁ , Nick J Wareham ₁₃₃ , Scott T Weiss ₁₂₅ , Wendy B White ₁₅₀ , Magnus Wickman _{91,

151} , Elisabeth Widén ₉₂ , Gonneke Willemsen ₁₄ , L Keoki Williams _{152,

153} , Inge M Wouters ₄₃ , James J Yang ₁₅₄ , Jing Hua Zhao ₁₃₃ , Miriam F Moffatt ₄ , Carole Ober ₁₅₅ , Dan L Nicolae ₁₅₆

Affiliation

Genetic Variation and Human Diseases Unit (UMR-946), Institut National de la Santé et de la Recherche Médicale (INSERM), Paris, France.
Institut Universitaire d'Hématologie, Université Paris Diderot, Université Sorbonne Paris Cité, Paris, France.
Division of Biomedical Informatics and Personalized Medicine, Colorado Center for Personalized Medicine, University of Colorado, Denver, CO, USA.
Section of Genomic Medicine, National Heart and Lung Institute, London, UK.
Cologne Center for Genomics and Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany.
School of Women's and Infants' Health, University of Western Australia, Perth, Western Australia, Australia.
Departments of Medicine and Epidemiology, Columbia University, New York, NY, USA.
Division of Genetic Epidemiology, Department of Epidemiology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, USA.
Department of Pediatrics and Child Health, University of Manitoba, Winnipeg, Manitoba, Canada.
Department of the Diagnostic Genomics Laboratory, PathWest Laboratory Medicine, Queen Elizabeth II Medical Centre, Nedlands, Western Australia, Australia.
Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, Denmark.
Department of Medicine, Landspitali, National University Hospital of Iceland, Reykjavik, Iceland.
Center for Genomics, Wake Forest University School of Medicine, Winston-Salem, NC, USA.
Department of Biological Psychology, Amsterdam Public Health Research Institute, Vrjie Universiteit, Amsterdam, The Netherlands.
University of Leicester, Institute for Lung Health, Glenfield Hospital, Leicester, UK.
Department of Respiratory Medicine, Ghent University Hospital, Ghent, Belgium.
Department of Epidemiology, Erasmus MC-University Medical Center Rotterdam, Rotterdam, The Netherlands.
Department of Respiratory Medicine, Erasmus MC-University Medical Center Rotterdam, Rotterdam, The Netherlands.
Department of Bioengineering & Therapeutic Sciences and Medicine, University of California, San Francisco, San Francisco, CA, USA.
Division of Pulmonary, Allergy and Critical Care, College of Physicians and Surgeons, Columbia University, New York, NY, USA.
National Heart and Lung Institute, Imperial College London, London, UK.
Royal Brompton Harefield National Health Service (NHS) Foundation Trust, London, UK.
Department of Medicine, University of British Columbia, Vancouver, British Columbia, Canada.
Biomedical Research Unit, Royal Brompton & Harefield National Health Service (NHS) Trust, London, UK.
Department of Epidemiology and Biostatistics, Imperial College London, London, UK.
Division of Infection, Immunity and Respiratory Medicine, School of Biological Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK.
Department of Paediatrics, Imperial College London, London, UK.
Centre for Heart and Lung Innovation, University of British Columbia, Vancouver, BC, Canada.
Department of Pediatrics, Division of Respiratory Medicine, Erasmus MC-University Medical Center Rotterdam, Rotterdam, The Netherlands.
Hospital Infantil de Mexico Federico Gomez, Mexico City, Mexico.
Department of Pediatrics, Division of Respiratory Medicine, and Department of Pediatrics, Division of Neonatology, Erasmus MC-University Medical Center Rotterdam, Rotterdam, The Netherlands.
Department of Medicine, University of California, San Francisco, San Francisco, CA, USA.
Department of General Practice and Primary Health Care, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
Division of Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, UK.
Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK.
Institute of Biochemistry and Genetics, Ufa Scientific Center of the Russian Academy of Sciences, Ufa, Russian Federation.
Department of Epidemiology Research, Statens Serum Institut, Copenhagen, Denmark.
Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.
Population Genetics Laboratory, Research Institute of Medical Genetics, Tomsk NRMC, Tomsk, Russian Federation.
Divisions of Genetics and Endocrinology, Children's Hospital, Boston, MA, USA.
Broad Institute, Cambridge, MA, USA.
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Division of Environmental Epidemiology, Institute for Risk Assessment Sciences, Utrecht University, Utrecht, The Netherlands.
Institute of Epidemiology and Medical Biometry, Ulm University, Ulm, Germany.
Department of Medicine, University of Washington, Seattle, WA, USA.
Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK.
MRC Integrative Epidemiology Unit, University of Bristol, Bristol, UK.
Asthma and Airway Disease Research Center and BIO5 Institute, University of Arizona, Tucson, AZ, USA.
deCODE genetics, Amgen Inc., Reykjavik, Iceland.
School of Engineering and Natural Sciences, University of Iceland, Reykjavik, Iceland.
Skin and Allergy Hospital, University of Helsinki, Helsinki, Finland.
Department of Epidemiology, University of Washington, Seattle, WA, USA.
Institute and Outpatient Clinic for Occupational, Social and Environmental Medicine, University Hospital in Munich, Munich, Germany.
Institute of Epidemiology I, Helmholtz Zentrum München, German Research Centre for Environmental Health, Neuherberg, Germany.
National Institute for Health and Welfare (THL), Helsinki, Finland.
Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania, Philadelphia, PA, USA.
Health Center, Department of Internal Medicine, Keio University, Tokyo, Japan.
Division of Endocrinology and Center for Basic and Translational Obesity Research, Boston Children's Hospital, Boston, MA, USA.
Departments of Pediatrics and Genetics, Harvard Medical School, Boston, MA, USA.
Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Cell Biology Telethon Kids Institute, University of Western Australia, Subiaco, Western Australia, Australia.
Ontario Institute for Cancer Research, Toronto, Ontario, Canada.
AbbVie Inc., Redwood City, CA, USA.
Busselton Population Medical Research Institute, Perth, Western Australia, Australia.
School of Population and Global Health, University of Western Australia, Nedlands, Western Australia, Australia.
Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland.
University of Basel, Basel, Switzerland.
Department of Biology, Medical Genetics and Ecology, Kursk State Medical University, Kursk, Russian Federation.
The Generation R Study Group, Department of Pediatrics and Department of Epidemiology, Erasmus MC-University Medical Center Rotterdam, Rotterdam, The Netherlands.
Department of Pulmonary Physiology and Sleep Medicine, Busselton Population Medical Research Institute, Sir Charles Gairdner Hospital, Nedlands, Western Australia, Australia.
School of Medicine and Pharmacology, University of Western Australia, Crawley, Western Australia, Australia.
Department of Medical Sciences: Respiratory, Allergy & Sleep Research, Uppsala University, Uppsala, Sweden.
Department of Epidemiology and Biostatistics, MRC-PHE Centre for Environment & Health, School of Public Health, Imperial College London, London, UK.
Center for Life Course Health Research, Faculty of Medicine, University of Oulu, Oulu, Finland.
Biocenter Oulu, University of Oulu, Oulu, Finland.
Unit of Primary Care, Oulu University Hospital, Oulu, Finland.
MRC-PHE Centre for Environment and Health, Imperial College London, London, UK.
School of Science and Health, Western Sydney University, Sydney, New South Wales, Australia.
Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
Department of Pediatric Pneumology and Allergy, University Children's Hospital Regensburg (KUNO), Regensburg, Germany.
Department of Clinical Physiology, University of Tampere and Tampere University Hospital, Tampere, Finland.
Department of Anesthesiology, Perioperative and Pain Medicine, Division of Critical Care Medicine, Boston Children's Hospital, Boston, MA, USA.
Department of Anaesthesia, Harvard Medical School, Boston, MA, USA.
Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russian Federation.
University of Groningen, University Medical Center Groningen, Department of Pediatric Pulmonology and Pediatric Allergology, Beatrix Children's Hospital, Groningen, The Netherlands.
Groningen Research Institute for Asthma and COPD (GRIAC), Groningen, The Netherlands.
Department of Pediatrics, University of Alberta, Edmonton, Alberta, Canada.
RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA.
Divison of Allergy and Clinical Immunology, Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Helsinki, Finland.
Pharmaceutical Care Unit, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium.
Department of Pulmonary Medicine, University of Turku and Turku University Hospital, Turku, Finland.
Département des Sciences Fondamentales, Université du Québec à Chicoutimi, Chicoutimi, Quebec, Canada.
Centre de Santé et de Services Sociaux du Saguenay-Lac-Saint-Jean, Saguenay, QC, Canada.
McGill University and Genome Quebec Innovation Centre, Montréal, QC, Canada.
Pediatric Pneumology and Immunology, Charité Universitätsmedizin, Berlin, Germany.
Max-Delbrück-Centrum (MDC) for Molecular Medicine, Berlin, Germany.
Pediatric Allergology, Experimental and Clinical Research Center, Charité Universitätsmedizin, Berlin, Germany.
Department of Clinical Chemistry, Fimlab Laboratories, Faculty of Medicine and Life Sciences, University of Tampere, Tampere, Finland.
Department of Public Health Sciences, Henry Ford Health System, Detroit, MI, USA.
Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Division of General Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
National Institute of Environmental Health Sciences, National Institutes of Health, Department of Health and Human Services, Research Triangle Park, NC, USA.
Center for Public Health Genomics, University of Virginia, Charlottesville, VA, USA.
Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia.
Division of Allergy & Clinical Immunology, Department of Medicine, Johns Hopkins University, Baltimore, MD, USA.
Department of Allergy and Clinical Immunology, National Research Institute for Child Health and Development, Tokyo, Japan.
Bristol Bioresource Laboratories, School of Social and Community Medicine, University of Bristol, Bristol, UK.
Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA.
Centre for Occupational and Environmental Medicine, Stockholm County Council, Stockholm, Sweden.
Sachs Children's Hospital, Stockholm, Sweden.
Department of Respiratory Medicine, Sir Charles Gairdner Hospital, Nedlands, Western Australia, Australia.
Schools of Population Health and of Medicine and Pharmacology, University of Western Australia, Perth, Western Australia, Australia.
Center for Applied Genomics and Precision Medicine, Duke University School of Medicine, Durham, NC, USA.
University Medical Center Groningen, Department of Pulmonology, University of Groningen, Groningen, The Netherlands.
Department of Medical Genetics, Faculty of Medicine, University of Tsukuba, Tsukuba, Japan.
Pulmonary Center, Department of Medicine, Boston University School of Medicine, Boston, MA, USA.
The National Heart, Lung, and Blood Institute's Framingham Heart Study, Framingham, MA, USA.
Department of Faculty Pediatrics, Siberian State Medical University, Tomsk, Russian Federation.
Analytic and Translational Genetics Unit, Departments of Medicine, of Neurology and of Psychiatry, Massachusetts General Hospital, Boston, MA, USA.
The Stanley Center for Psychiatric Research and Program in Medical and Population Genetics, Broad Institute, Cambridge, MA, USA.
Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
Department of Clinical Physiology and Nuclear Medicine, University of Turku and Turku University Hospital, Turku, Finland.
Department of Medical and Molecular Genetics, King's College London, London, UK.
Respiratory Medicine, Murdoch Children's Research Institute, Melbourne, Victoria, Australia.
Hubert Department of Global Health, Mory University, Atlanta, GA, USA.
Center for Population Health Research, National Institute of Public Health, Cuernavaca, Mexico.
Department of Psychiatry, Kern Medical, Bakersfield, CA, USA.
Department of Public Health, Section for Environment, Occupation & Health, Aarhus University, Aarhus, Denmark.
MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, UK.
Department of Faculty Therapy, Siberian State Medical University, Tomsk, Russian Federation.
University Hospital of South Manchester, National Health Service (NHS) Foundation Trust, Manchester, UK.
Institut National de la Santé et de la Recherche Médicale (INSERM) U1209, Institute for Advanced Biosciences, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, France.
Université de Grenoble Alpes/CNRS UMR5309, Institute for Advanced Biosciences, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, France.
Division of Pulmonary and Critical Care Medicine, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA.
Population Health Research Institute, St George's University of London, London, UK.
Netherlands Healthcare Inspectorate, The Hague, The Netherlands.
Department of Internal Medicine, Erasmus MC-University Medical Center Rotterdam, Rotterdam, The Netherlands.
Institute for Respiratory Health and Harry Perkins Institute of Medical Research, University of Western Australia and The Lung Health Clinic, Nedlands, Western Australia, Australia.
Division of Metabolic Diseases and Nutritional Medicine, Dr. von Hauner Children's Hospital, Ludwig-Maximilians-University of Munich, Munich, Germany.
Department of Medical Science Mathematics, Medical Research Institute, Tokyo Medical and Dental University, Tokyo, Japan.
The Generation R Study Group, Department of Pediatrics, Division of Respiratory Medicine and Department of Epidemiology, Erasmus MC-University Medical Center Rotterdam, Rotterdam, The Netherlands.
Department of Pediatrics, Marien-Hospital Wesel, Wesel, Germany.
Dr. Von Hauner Children's Hospital, Ludwig Maximilians University Munich, Munich, Germany.
German Center for Lung Research, Munich, Germany.
University of Groningen, University Medical Center Groningen, Department of Epidemiology, Groningen, The Netherlands.
Undergraduate Training and Education Center (UTEC), Jackson Heart Study, Tougaloo College, Jackson, MI, USA.
Centre for Clinical Research Sörmland, Uppsala University, Eskilstuna, Sweden.
Center for Health Policy and Health Services Research, Henry Ford Health System, Detroit, MI, USA.
Department of Internal Medicine, Henry Ford Health System, Detroit, MI, USA.
School of Nursing, University of Michigan, Ann Arbor, MI, USA.
Department of Human Genetics, University of Chicago, Chicago, IL, USA.
Departments of Statistics, Human Genetics and Medicine, Section of Genetic Medicine, University of Chicago, Chicago, IL, USA.

We examined common variation in asthma risk by conducting a meta-analysis of worldwide asthma genome-wide association studies (23,948 asthma cases, 118,538 controls) of individuals from ethnically diverse populations. We identified five new asthma loci, found two new associations at two known asthma loci, established asthma associations at two loci previously implicated in the comorbidity of asthma plus hay fever, and confirmed nine known loci. Investigation of pleiotropy showed large overlaps in genetic variants with autoimmune and inflammatory diseases. The enrichment in enhancer marks at asthma risk loci, especially in immune cells, suggested a major role of these loci in the regulation of immunologically related mechanisms.

中文翻译：

多祖先关联研究确定了与免疫细胞增强标记共定位的新哮喘风险位点。

我们通过对来自不同种族人群的全球哮喘全基因组关联研究（23,948 例哮喘病例，118,538 例对照）进行荟萃分析，检查了哮喘风险的常见变异。我们确定了五个新的哮喘位点，在两个已知的哮喘位点发现了两个新的关联，在先前与哮喘加花粉症合并症有关的两个位点建立了哮喘关联，并确认了九个已知位点。对多效性的研究表明，遗传变异与自身免疫性疾病和炎症性疾病有很大的重叠。哮喘风险位点（尤其是免疫细胞中）增强子标记的富集表明这些位点在免疫学相关机制的调节中起主要作用。

更新日期：2017-12-22

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