Meta-Analysis

. 2013 Aug;45(8):912-917.

doi: 10.1038/ng.2676. Epub 2013 Jun 23.

Genome-wide meta-analysis identifies new susceptibility loci for migraine

Verneri Anttila^#^{1

2

3

4}, Bendik S Winsvold^#^{1

5}, Padhraig Gormley¹, Tobias Kurth^{6

7

8}, Francesco Bettella⁹, George McMahon¹⁰, Mikko Kallela¹¹, Rainer Malik¹², Boukje de Vries¹³, Gisela Terwindt¹⁴, Sarah E Medland¹⁵, Unda Todt¹⁶, Wendy L McArdle¹⁰, Lydia Quaye¹⁷, Markku Koiranen¹⁸, M Arfan Ikram^{19

20

21}, Terho Lehtimäki²², Anine H Stam¹⁴, Lannie Ligthart^{23

24}, Juho Wedenoja²⁵, Ian Dunham²⁶, Benjamin M Neale^{3

4}, Priit Palta^{1

2}, Eija Hamalainen^{1

2}, Markus Schürks²⁷, Lynda M Rose⁸, Julie E Buring⁸, Paul M Ridker^{8

28}, Stacy Steinberg⁹, Hreinn Stefansson⁹, Finnbogi Jakobsson²⁹, Debbie A Lawlor¹⁰, David M Evans¹⁰, Susan M Ring¹⁰, Markus Färkkilä¹¹, Ville Artto¹¹, Mari A Kaunisto^{2

30}, Tobias Freilinger^{12

31}, Jean Schoenen³², Rune R Frants¹³, Nadine Pelzer¹⁴, Claudia M Weller¹³, Ronald Zielman¹⁴, Andrew C Heath³³, Pamela A F Madden³³, Grant W Montgomery¹⁵, Nicholas G Martin¹⁵, Guntram Borck¹⁶, Hartmut Göbel³⁴, Axel Heinze³⁴, Katja Heinze-Kuhn³⁴, Frances M K Williams¹⁷, Anna-Liisa Hartikainen³⁵, Anneli Pouta^{18

35

36}, Joyce van den Ende¹⁹, Andre G Uitterlinden³⁷, Albert Hofman³⁸, Najaf Amin¹⁹, Jouke-Jan Hottenga²³, Jacqueline M Vink²³, Kauko Heikkilä²⁵, Michael Alexander^{39

40}, Bertram Muller-Myhsok^{41

42}, Stefan Schreiber^{43

44}, Thomas Meitinger^{45

46}, Heinz Erich Wichmann^{47

48

49}, Arpo Aromaa⁵⁰, Johan G Eriksson^{30

50

51

52

53}, Bryan Traynor⁵⁴, Daniah Trabzuni^{55

56}; North American Brain Expression Consortium; UK Brain Expression Consortium; Elizabeth Rossin^{3

4

57}, Kasper Lage^{3

4

58

59

60}, Suzanne B R Jacobs⁴, J Raphael Gibbs^{54

55}, Ewan Birney²⁶, Jaakko Kaprio^{2

61

25}, Brenda W Penninx^{62

24

63

64}, Dorret I Boomsma²³, Cornelia van Duijn¹⁹, Olli Raitakari^{65

66}, Marjo-Riitta Jarvelin^{67

18

68

36}, John-Anker Zwart⁵, Lynn Cherkas¹⁷, David P Strachan⁶⁹, Christian Kubisch¹⁶, Michel D Ferrari¹⁴, Arn M J M van den Maagdenberg^{13

14}, Martin Dichgans^{12

42}, Maija Wessman^{2

30}, George Davey Smith¹⁰, Kari Stefansson^{9

70}, Mark J Daly^{3

4}, Dale R Nyholt¹⁵, Daniel Chasman^{8

28}, Aarno Palotie^{1

2

4}

Collaborators, Affiliations

Collaborators

Sampath Arepalli, Mark R Cookson, Allissa Dillman, Luigi Ferrucci, J Raphael Gibbs, Dena G Hernandez, Robert Johnson, Dan L Longo, Michael A Nalls, Richard O'Brien, Andrew Singleton, Bryan Traynor, Juan Troncoso, Marcel van der Brug, H R Zielke, Alan B Zonderman, John A Hardy, Mina Ryten, Colin Smith, Daniah Trabzuni, Robert Walker, Mike E Weale, Verneri Anttila, Bendik S Winsvold, Padhraig Gormley, Tobias Kurth, Francesco Bettella, George McMahon, Mikko Kallela, Rainer Malik, Boukje de Vries, Gisela Terwindt, Unda Todt, Lydia Quaye, Priit Palta, Eija Hämäläinen, Markus Schürks, Stacy Steinberg, Hreinn Stefansson, Markus Färkkilä, Ville Artto, Mari A Kaunisto, Tobias Freilinger, Jean Schoenen, Rune R Frants, Guntram Borck, Hartmut Göbel, Axel Heinze, Katja Heinze-Kuhn, Bertram Muller-Myhsok, Jaakko Kaprio, John-Anker Zwart, Lynn Cherkas, David P Strachan, Christian Kubisch, Michel D Ferrari, Arn M J M van den Maagdenberg, Martin Dichgans, Maija Wessman, George Davey Smith, Dale R Nyholt, Daniel Chasman, Aarno Palotie

Affiliations

¹ Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, UK.
² Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Helsinki, Finland.
³ Analytical and Translational Genetics Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
⁴ Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
⁵ Department of Neurology, Oslo University Hospital and University of Oslo, Oslo, Norway.
⁶ INSERM Unit 708 - Neuroepidemiology, F-33000 Bordeaux, France.
⁷ University of Bordeaux, F-33000 Bordeaux, France.
⁸ Division of Preventive Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, USA.
⁹ deCODE genetics, Reykjavik, Iceland.
¹⁰ MRC Centre for Causal Analyses in Translational Epidemiology, School of Social and Community Medicine, University of Bristol, Bristol, UK.
¹¹ Department of Neurology, Helsinki University Central Hospital, Helsinki, Finland.
¹² Institute for Stroke and Dementia Research, Klinikum der Universität München, Ludwig-Maximilians-Universität, Munich, Germany.
¹³ Department of Human Genetics, Leiden University Medical Centre, Leiden, The Netherlands.
¹⁴ Department of Neurology, Leiden University Medical Centre, Leiden, The Netherlands.
¹⁵ Queensland Institute of Medical Research, Brisbane, Queensland, Australia.
¹⁶ Institute of Human Genetics, University of Ulm, Ulm, Germany.
¹⁷ Department of Twin Research and Genetic Epidemiology, King's College London, London, UK.
¹⁸ Institute of Health Sciences, University of Oulu, Oulu, Finland.
¹⁹ Genetic Epidemiology Unit, Department of Epidemiology, Erasmus University Medical Center, Rotterdam, the Netherlands.
²⁰ Department of Radiology Erasmus University Medical Centre, Rotterdam, The Netherlands.
²¹ Department of Neurology Erasmus University Medical Centre, Rotterdam, The Netherlands.
²² Department of Clinical Chemistry, Fimlab Laboratories and University of Tampere School of Medicine, Tampere, Finland.
²³ Department of Biological Psychology, VU University, Amsterdam, The Netherlands.
²⁴ EMGO+ Institute for Health and Care Research, VU University Medical Center, Amsterdam, The Netherlands.
²⁵ Department of Public Health, Hjelt Institute, University of Helsinki, Helsinki, Finland.
²⁶ European Bioinformatics Insitute, Wellcome Trust Genome Campus, Cambridge, UK.
²⁷ Department of Neurology, University Hospital Essen, Essen, Germany.
²⁸ Harvard Medical School, Boston, MA 02215, USA.
²⁹ Department of Neurology, Landspitali University Hospital, Reykjavik, Iceland.
³⁰ Folkhälsan Research Center, Helsinki, Finland.
³¹ Department of Neurology, Klinikum der Universität München, Munich, Germany.
³² Headache Research Unit, Department of Neurology and Groupe Interdisciplinaire de Génoprotéomique Appliquée (GIGA)-Neurosciences, Liège University, Liège, Belgium.
³³ Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri, USA.
³⁴ Kiel Pain and Headache Center, Kiel, Germany.
³⁵ Department of Clinical Sciences/Obstetrics and Gynecology, University Hospital of Oulu, Oulu, Finland.
³⁶ Department of Children, Young People and Families, National Institute for Health and Welfare, Helsinki, Finland.
³⁷ Department of Internal Medicine, Erasmus Medical Center, Rotterdam, The Netherlands.
³⁸ Genetic Epidemiology Unit, Department of Clinical Genetics, Erasmus University Medical Centre, Rotterdam, The Netherlands.
³⁹ Department of Genomics, Life & Brain Center, University of Bonn, Bonn, Germany.
⁴⁰ Institute of Human Genetics, University of Bonn, Bonn, Germany.
⁴¹ Max Planck Institute of Psychiatry, Munich, Germany.
⁴² Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
⁴³ Department of Clinical Molecular Biology, Christian Albrechts University, Kiel, Germany.
⁴⁴ Department of Internal Medicine I, Christian Albrechts University, Kiel, Germany.
⁴⁵ Institute of Human Genetics, Helmholtz Center Munich, Neuherberg, Germany.
⁴⁶ Institute of Human Genetics, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany.
⁴⁷ Institut für Medizinische Informationsverarbeitung, Biometrie und Epidemiologie, Ludwig-Maximilians-Universität München, Munich, Germany.
⁴⁸ Institute of Epidemiology I, HelmholtzCenter Munich, Neuherberg, Germany.
⁴⁹ Klinikum Großhadern, Ludwig-Maximilians-Universität München, Munich, Germany.
⁵⁰ National Institute for Health and Welfare, Helsinki, Finland.
⁵¹ Department of General Practice, Helsinki University Central Hospital, Helsinki, Finland.
⁵² Vaasa Central Hospital, Vaasa, Finland.
⁵³ Department of General Practice and Primary Health Care, University of Helsinki, Helsinki, Finland.
⁵⁴ Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA.
⁵⁵ Department of Molecular Neuroscience, Institute of Neurology, University College London, London, UK.
⁵⁶ Department of Genetics, King Faisal Specialist Hospital and Research Centre, Riyadh, Saudi Arabia.
⁵⁷ Center for Human Genetic Research, Massachusetts General Hospital, Boston, MA, USA.
⁵⁸ Pediatric Surgical Research Laboratories, Massachusetts General Hospital for Children, Massachusetts General Hospital, Boston, MA, USA.
⁵⁹ Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, Lyngby, Denmark.
⁶⁰ Center for Protein Research, University of Copenhagen, Copenhagen, Denmark.
⁶¹ Department of Mental Health and Alcohol Research, National Institute for Health and Welfare, Helsinki, Finland.
⁶² Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands.
⁶³ Department of Psychiatry, University Medical Center Groningen, Groningen, The Netherlands.
⁶⁴ Department of Psychiatry, Leiden University Medical Center, Leiden, The Netherlands.
⁶⁵ Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, Turku University Hospital, Turku, Finland.
⁶⁶ Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku, Finland.
⁶⁷ Department of Epidemiology and Biostatistics, School of Public Health, MRC-HPA Centre for Environment and Health, Faculty of Medicine, Imperial College, London, UK.
⁶⁸ Biocenter Oulu, University of Oulu, Oulu, Finland.
⁶⁹ Division of Population Health Sciences and Education, St George's, University of London, London, UK.
⁷⁰ School of Medicine, University of Iceland, Reykjavik, Iceland.

^# Contributed equally.

PMID: 23793025
PMCID: PMC4041123
DOI: 10.1038/ng.2676

Meta-Analysis

Genome-wide meta-analysis identifies new susceptibility loci for migraine

Verneri Anttila et al. Nat Genet. 2013 Aug.

. 2013 Aug;45(8):912-917.

doi: 10.1038/ng.2676. Epub 2013 Jun 23.

Authors

Collaborators

Sampath Arepalli, Mark R Cookson, Allissa Dillman, Luigi Ferrucci, J Raphael Gibbs, Dena G Hernandez, Robert Johnson, Dan L Longo, Michael A Nalls, Richard O'Brien, Andrew Singleton, Bryan Traynor, Juan Troncoso, Marcel van der Brug, H R Zielke, Alan B Zonderman, John A Hardy, Mina Ryten, Colin Smith, Daniah Trabzuni, Robert Walker, Mike E Weale, Verneri Anttila, Bendik S Winsvold, Padhraig Gormley, Tobias Kurth, Francesco Bettella, George McMahon, Mikko Kallela, Rainer Malik, Boukje de Vries, Gisela Terwindt, Unda Todt, Lydia Quaye, Priit Palta, Eija Hämäläinen, Markus Schürks, Stacy Steinberg, Hreinn Stefansson, Markus Färkkilä, Ville Artto, Mari A Kaunisto, Tobias Freilinger, Jean Schoenen, Rune R Frants, Guntram Borck, Hartmut Göbel, Axel Heinze, Katja Heinze-Kuhn, Bertram Muller-Myhsok, Jaakko Kaprio, John-Anker Zwart, Lynn Cherkas, David P Strachan, Christian Kubisch, Michel D Ferrari, Arn M J M van den Maagdenberg, Martin Dichgans, Maija Wessman, George Davey Smith, Dale R Nyholt, Daniel Chasman, Aarno Palotie

Affiliations

¹ Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, UK.
² Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Helsinki, Finland.
³ Analytical and Translational Genetics Unit, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.
⁴ Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
⁵ Department of Neurology, Oslo University Hospital and University of Oslo, Oslo, Norway.
⁶ INSERM Unit 708 - Neuroepidemiology, F-33000 Bordeaux, France.
⁷ University of Bordeaux, F-33000 Bordeaux, France.
⁸ Division of Preventive Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, USA.
⁹ deCODE genetics, Reykjavik, Iceland.
¹⁰ MRC Centre for Causal Analyses in Translational Epidemiology, School of Social and Community Medicine, University of Bristol, Bristol, UK.
¹¹ Department of Neurology, Helsinki University Central Hospital, Helsinki, Finland.
¹² Institute for Stroke and Dementia Research, Klinikum der Universität München, Ludwig-Maximilians-Universität, Munich, Germany.
¹³ Department of Human Genetics, Leiden University Medical Centre, Leiden, The Netherlands.
¹⁴ Department of Neurology, Leiden University Medical Centre, Leiden, The Netherlands.
¹⁵ Queensland Institute of Medical Research, Brisbane, Queensland, Australia.
¹⁶ Institute of Human Genetics, University of Ulm, Ulm, Germany.
¹⁷ Department of Twin Research and Genetic Epidemiology, King's College London, London, UK.
¹⁸ Institute of Health Sciences, University of Oulu, Oulu, Finland.
¹⁹ Genetic Epidemiology Unit, Department of Epidemiology, Erasmus University Medical Center, Rotterdam, the Netherlands.
²⁰ Department of Radiology Erasmus University Medical Centre, Rotterdam, The Netherlands.
²¹ Department of Neurology Erasmus University Medical Centre, Rotterdam, The Netherlands.
²² Department of Clinical Chemistry, Fimlab Laboratories and University of Tampere School of Medicine, Tampere, Finland.
²³ Department of Biological Psychology, VU University, Amsterdam, The Netherlands.
²⁴ EMGO+ Institute for Health and Care Research, VU University Medical Center, Amsterdam, The Netherlands.
²⁵ Department of Public Health, Hjelt Institute, University of Helsinki, Helsinki, Finland.
²⁶ European Bioinformatics Insitute, Wellcome Trust Genome Campus, Cambridge, UK.
²⁷ Department of Neurology, University Hospital Essen, Essen, Germany.
²⁸ Harvard Medical School, Boston, MA 02215, USA.
²⁹ Department of Neurology, Landspitali University Hospital, Reykjavik, Iceland.
³⁰ Folkhälsan Research Center, Helsinki, Finland.
³¹ Department of Neurology, Klinikum der Universität München, Munich, Germany.
³² Headache Research Unit, Department of Neurology and Groupe Interdisciplinaire de Génoprotéomique Appliquée (GIGA)-Neurosciences, Liège University, Liège, Belgium.
³³ Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri, USA.
³⁴ Kiel Pain and Headache Center, Kiel, Germany.
³⁵ Department of Clinical Sciences/Obstetrics and Gynecology, University Hospital of Oulu, Oulu, Finland.
³⁶ Department of Children, Young People and Families, National Institute for Health and Welfare, Helsinki, Finland.
³⁷ Department of Internal Medicine, Erasmus Medical Center, Rotterdam, The Netherlands.
³⁸ Genetic Epidemiology Unit, Department of Clinical Genetics, Erasmus University Medical Centre, Rotterdam, The Netherlands.
³⁹ Department of Genomics, Life & Brain Center, University of Bonn, Bonn, Germany.
⁴⁰ Institute of Human Genetics, University of Bonn, Bonn, Germany.
⁴¹ Max Planck Institute of Psychiatry, Munich, Germany.
⁴² Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
⁴³ Department of Clinical Molecular Biology, Christian Albrechts University, Kiel, Germany.
⁴⁴ Department of Internal Medicine I, Christian Albrechts University, Kiel, Germany.
⁴⁵ Institute of Human Genetics, Helmholtz Center Munich, Neuherberg, Germany.
⁴⁶ Institute of Human Genetics, Klinikum Rechts der Isar, Technische Universität München, Munich, Germany.
⁴⁷ Institut für Medizinische Informationsverarbeitung, Biometrie und Epidemiologie, Ludwig-Maximilians-Universität München, Munich, Germany.
⁴⁸ Institute of Epidemiology I, HelmholtzCenter Munich, Neuherberg, Germany.
⁴⁹ Klinikum Großhadern, Ludwig-Maximilians-Universität München, Munich, Germany.
⁵⁰ National Institute for Health and Welfare, Helsinki, Finland.
⁵¹ Department of General Practice, Helsinki University Central Hospital, Helsinki, Finland.
⁵² Vaasa Central Hospital, Vaasa, Finland.
⁵³ Department of General Practice and Primary Health Care, University of Helsinki, Helsinki, Finland.
⁵⁴ Laboratory of Neurogenetics, National Institute on Aging, National Institutes of Health, Bethesda, MD, USA.
⁵⁵ Department of Molecular Neuroscience, Institute of Neurology, University College London, London, UK.
⁵⁶ Department of Genetics, King Faisal Specialist Hospital and Research Centre, Riyadh, Saudi Arabia.
⁵⁷ Center for Human Genetic Research, Massachusetts General Hospital, Boston, MA, USA.
⁵⁸ Pediatric Surgical Research Laboratories, Massachusetts General Hospital for Children, Massachusetts General Hospital, Boston, MA, USA.
⁵⁹ Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, Lyngby, Denmark.
⁶⁰ Center for Protein Research, University of Copenhagen, Copenhagen, Denmark.
⁶¹ Department of Mental Health and Alcohol Research, National Institute for Health and Welfare, Helsinki, Finland.
⁶² Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands.
⁶³ Department of Psychiatry, University Medical Center Groningen, Groningen, The Netherlands.
⁶⁴ Department of Psychiatry, Leiden University Medical Center, Leiden, The Netherlands.
⁶⁵ Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, Turku University Hospital, Turku, Finland.
⁶⁶ Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku, Finland.
⁶⁷ Department of Epidemiology and Biostatistics, School of Public Health, MRC-HPA Centre for Environment and Health, Faculty of Medicine, Imperial College, London, UK.
⁶⁸ Biocenter Oulu, University of Oulu, Oulu, Finland.
⁶⁹ Division of Population Health Sciences and Education, St George's, University of London, London, UK.
⁷⁰ School of Medicine, University of Iceland, Reykjavik, Iceland.

^# Contributed equally.

PMID: 23793025
PMCID: PMC4041123
DOI: 10.1038/ng.2676

Abstract

Migraine is the most common brain disorder, affecting approximately 14% of the adult population, but its molecular mechanisms are poorly understood. We report the results of a meta-analysis across 29 genome-wide association studies, including a total of 23,285 individuals with migraine (cases) and 95,425 population-matched controls. We identified 12 loci associated with migraine susceptibility (P<5×10(-8)). Five loci are new: near AJAP1 at 1p36, near TSPAN2 at 1p13, within FHL5 at 6q16, within C7orf10 at 7p14 and near MMP16 at 8q21. Three of these loci were identified in disease subgroup analyses. Brain tissue expression quantitative trait locus analysis suggests potential functional candidate genes at four loci: APOA1BP, TBC1D7, FUT9, STAT6 and ATP5B.

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Figures

**Figure 1. Description of the studies comprising the International Migraine Genetics Meta-analysis Consortium, and their sample contributions to each analysis**
Each coloured box corresponds to one analysed phenotype and lists the total number of cases and controls, as well as the sample contributions of individual cohorts. Participation in each analysis depended on the availability of the data in question and the recruitment method.

**Figure 2. Manhattan plot of the results of the meta-analysis**
Results of the meta-analysis of all migraine cases, of any migraine subtype or recruiting method, versus all available controls, adjusting for gender. Red dots indicate SNPs with significant (< 5 × 10⁻⁸) P values. A) All migraine (23 285 cases, 95 425 controls) B) Clinic-based studies only (5 175 cases, 13 972 controls) C) Migraine with aura (5 118 cases, 74 239 controls) D) Migraine without aura (7 107 cases, 69 427 controls)

See this image and copyright information in PMC

Comment in

Migrane: new susceptibility loci associated with migraine.
Jones B. Jones B. Nat Rev Neurol. 2013 Aug;9(8):419. doi: 10.1038/nrneurol.2013.136. Epub 2013 Jul 9. Nat Rev Neurol. 2013. PMID: 23835538 No abstract available.

References

1. Anttila V, et al. Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1. Nat Genet. 2010;42:869–73. - PMC - PubMed
1. Chasman DI, et al. Genome-wide association study reveals three susceptibility loci for common migraine in the general population. Nat Genet. 2011;43:695–8. - PMC - PubMed
1. Ligthart L, et al. Meta-analysis of genome-wide association for migraine in six population-based European cohorts. Eur J Hum Genet. 2011;19:901–7. - PMC - PubMed
1. Freilinger T, et al. Genome-wide association analysis identifies susceptibility loci for migraine without aura. Nat Genet. 2012;44:777–82. - PMC - PubMed
1. International Headache Society The International Classification of Headache Disorders: 2nd edition. Cephalalgia. 2004;24(Suppl 1):9–160. - PubMed

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Genome-wide meta-analysis identifies new susceptibility loci for migraine

Collaborators

Affiliations

Genome-wide meta-analysis identifies new susceptibility loci for migraine

Authors

Collaborators

Affiliations

Abstract

Figures

Comment in

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical

Molecular Biology Databases

Research Materials

Miscellaneous