Divya Mehta1, Felix C Tropf2, Jacob Gratten1, Andrew Bakshi1, Zhihong Zhu1, Silviu-Alin Bacanu3, Gibran Hemani4, Patrik K E Magnusson5, Nicola Barban6, Tõnu Esko7, Andres Metspalu7, Harold Snieder8, Bryan J Mowry9, Kenneth S Kendler10, Jian Yang1, Peter M Visscher1, John J McGrath1, Melinda C Mills6, Naomi R Wray1, S Hong Lee11, Ole A Andreassen12, Elvira Bramon13, Richard Bruggeman14, Joseph D Buxbaum15, Murray J Cairns16, Rita M Cantor17, C Robert Cloninger18, David Cohen19, Benedicto Crespo-Facorro20, Ariel Darvasi21, Lynn E DeLisi22, Timothy Dinan23, Srdjan Djurovic24, Gary Donohoe25, Elodie Drapeau26, Valentina Escott-Price27, Nelson B Freimer28, Lyudmila Georgieva27, Lieuwe de Haan29, Frans A Henskens30, Inge Joa31, Antonio Julià32, Andrey Khrunin33, Bernard Lerer34, Svetlana Limborska33, Carmel M Loughland35, Milan Macek36, Patrik K E Magnusson5, Sara Marsal32, Robert W McCarley37, Andrew M McIntosh38, Andrew McQuillin39, Bela Melegh40, Patricia T Michie41, Derek W Morris25, Kieran C Murphy42, Inez Myin-Germeys43, Ann Olincy44, Jim Van Os45, Christos Pantelis46, Danielle Posthuma47, Digby Quested48, Ulrich Schall35, Rodney J Scott49, Larry J Seidman50, Draga Toncheva51, Paul A Tooney52, John Waddington53, Daniel R Weinberger54, Mark Weiser55, Jing Qin Wu56. 1. Queensland Brain Institute, The University of Queensland, Brisbane, Australia. 2. Department of Sociology, Interuniversity Center for Social Science Theory and Methodology, University of Groningen, Groningen, the Netherlands3Department of Sociology, Nuffield College, University of Oxford, Oxford, England. 3. Virginia Institute of Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond5Department of Psychiatry, Virginia Commonwealth University, Richmond. 4. Medical Research Council Integrative Epidemiology Unit, School of Social and Community Medicine, University of Bristol, Bristol, England. 5. Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden. 6. Department of Sociology, Nuffield College, University of Oxford, Oxford, England. 7. Estonian Genome Center, University of Tartu, Tartu, Estonia. 8. Department of Epidemiology, University of Groningen, The University Medical Center Groningen, Groningen, the Netherlands. 9. Queensland Brain Institute, The University of Queensland, Brisbane, Australia10Queensland Centre for Mental Health Research, Wacol, Australia. 10. Virginia Institute of Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond5Department of Psychiatry, Virginia Commonwealth University, Richmond11Department of Human and Molecular Genetics, Virginia Commonwealth University, Richm. 11. Queensland Brain Institute, The University of Queensland, Brisbane, Australia12School of Environmental and Rural Science, University of New England, Armidale, Australia. 12. NORMENT, KG Jebsen Centre for Psychosis Research, Institute of Clinical Medicine, University of Oslo, Oslo, Norway14Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway. 13. University College London, London, England. 14. University Medical Center Groningen, Department of Psychiatry, University of Groningen, Groningen, the Netherlands. 15. Department of Human Genetics, Icahn School of Medicine at Mount Sinai, New York, New York18Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, New York19Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York. 16. Schizophrenia Research Institute, Sydney, Australia22Priority Centre for Translational Neuroscience and Mental Health, University of Newcastle, Newcastle, Australia23School of Biomedical Sciences and Pharmacy, University of Newcastle, Callaghan, Australia. 17. Department of Human Genetics, David Geffen School of Medicine, University of California, Los Angeles. 18. Department of Psychiatry, Washington University in St Louis, St Louis, Missouri. 19. Department of Child and Adolescent Psychiatry, Assistance Publique Hôpitaux de Paris, Pierre and Marie Curie University, and Institute for Intelligent Systems and Robotics, Paris, France. 20. CIBERSAM, University Hospital Marqués de Valdecilla, University of Cantabria-IDIVAL, Department of Psychiatry, Santander, Spain28 Centro Investigación Biomédica en Red Salud Mental, Madrid, Spain. 21. Department of Genetics, The Hebrew University of Jerusalem, Jerusalem, Israel. 22. Schizophrenia Research Institute, Sydney, Australia30VA Boston Health Care System, Brockton, Massachusetts. 23. Department of Psychiatry, University College Cork, Cork, Ireland. 24. NORMENT, KG Jebsen Centre for Psychosis Research, Department of Clinical Science, University of Bergen, Bergen, Norway33Department of Medical Genetics, Oslo University Hospital, Oslo, Norway. 25. Cognitive Genetics and Therapy Group, School of Psychology and Discipline of Biochemistry, National University of Ireland Galway, Galway, Ireland35Neuropsychiatric Genetics Research Group, Department of Psychiatry, Trinity College Dublin, Dublin, Ireland. 26. Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, New York. 27. MRC Centre for Neuropsychiatric Genetics and Genomics, Institute of Psychological Medicine and Clinical Neurosciences, School of Medicine, Cardiff University, Cardiff, Wales. 28. Center for Neurobehavioral Genetics, Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles. 29. Department of Psychiatry, Academic Medical Centre, University of Amsterdam, Amsterdam, the Netherlands. 30. Schizophrenia Research Institute, Sydney, Australia39School of Electrical Engineering and Computer Science, University of Newcastle, Newcastle, Australia40Priority Research Centre for Health Behaviour, University of Newcastle, Newcastle, Australia. 31. Regional Centre for Clinical Research in Psychosis, Department of Psychiatry, Stavanger University Hospital, Stavanger, Norway. 32. Rheumatology Research Group, Vall d'Hebron Research Institute, Barcelona, Spain. 33. Institute of Molecular Genetics, Russian Academy of Sciences, Moscow, Russia. 34. Department of Psychiatry, Hadassah-Hebrew University Medical Center, Jerusalem, Israel. 35. Schizophrenia Research Institute, Sydney, Australia22Priority Centre for Translational Neuroscience and Mental Health, University of Newcastle, Newcastle, Australia. 36. Department of Biology and Medical Genetics, Second Faculty of Medicine and University Hospital Motol, Prague, Czech Republic. 37. VA Boston Health Care System, Brockton, Massachusetts47Department of Psychiatry, Harvard Medical School, Boston, Massachusetts. 38. Division of Psychiatry, University of Edinburgh, Edinburgh, Scotland49Centre for Cognitive Ageing and Cognitive Epidemiology, University of Edinburgh, Edinburgh, Scotland. 39. Molecular Psychiatry Laboratory, Division of Psychiatry, University College London, London, England. 40. Department of Medical Genetics, University of Pécs, Pécs, Hungary52Szentagothai Research Center, University of Pécs, Pécs, Hungary. 41. Schizophrenia Research Institute, Sydney, Australia53School of Psychology, University of Newcastle, Newcastle, Australia. 42. Department of Psychiatry, Royal College of Surgeons in Ireland, Dublin, Ireland. 43. Center for Contextual Psychiatry, Department of Neuroscience, KU Leuven, Leuven, Belgium. 44. Department of Psychiatry, University of Colorado Denver, Aurora. 45. Institute of Psychiatry, King's College London, London, England58Maastricht University Medical Centre, South Limburg Mental Health Research and Teaching Network, EURON, Maastricht, the Netherlands. 46. Schizophrenia Research Institute, Sydney, Australia59Melbourne Neuropsychiatry Centre, Department of Psychiatry, University of Melbourne and Melbourne Health, Melbourne, Australia. 47. Department of Functional Genomics, Center for Neurogenomics and Cognitive Research, Neuroscience Campus Amsterdam, VU University, Amsterdam, the Netherlands61Department of Complex Trait Genetics, Neuroscience Campus Amsterdam, VU University Medical Center. 48. Department of Psychiatry, University of Oxford, Oxford, England. 49. Schizophrenia Research Institute, Sydney, Australia23School of Biomedical Sciences and Pharmacy, University of Newcastle, Callaghan, Australia64Hunter New England Health Service, Newcastle, Australia. 50. Department of Psychiatry, Harvard Medical School, Boston, Massachusetts65Massachusetts Mental Health Center Public Psychiatry Division, Beth Israel Deaconess Medical Center, Boston. 51. Department of Medical Genetics, Medical University, Sofia, Bulgaria. 52. Schizophrenia Research Institute, Sydney, Australia23School of Biomedical Sciences and Pharmacy, University of Newcastle, Callaghan, Australia67Priority Research Centre for Translational Neuroscience and Mental Health, University of Newcastle, Newcastle. 53. Molecular and Cellular Therapeutics, Royal College of Surgeons in Ireland, Dublin, Ireland. 54. Lieber Institute for Brain Development, Baltimore, Maryland70Department of Psychiatry and Behavioral Sciences, The Johns Hopkins School of Medicine, Baltimore, Maryland71Department of Neurology, The Johns Hopkins School of Medicine, Baltimore, Maryland72. 55. Sheba Medical Center, Tel Hashomer, Israel. 56. Schizophrenia Research Institute, Sydney, Australia23School of Biomedical Sciences and Pharmacy, University of Newcastle, Callaghan, Australia.
Abstract
IMPORTANCE: A recently published study of national data by McGrath et al in 2014 showed increased risk of schizophrenia (SCZ) in offspring associated with both early and delayed parental age, consistent with a U-shaped relationship. However, it remains unclear if the risk to the child is due to psychosocial factors associated with parental age or if those at higher risk for SCZ tend to have children at an earlier or later age. OBJECTIVE: To determine if there is a genetic association between SCZ and age at first birth (AFB) using genetically informative but independently ascertained data sets. DESIGN, SETTING, AND PARTICIPANTS: This investigation used multiple independent genome-wide association study data sets. The SCZ sample comprised 18 957 SCZ cases and 22 673 controls in a genome-wide association study from the second phase of the Psychiatric Genomics Consortium, and the AFB sample comprised 12 247 genotyped women measured for AFB from the following 4 community cohorts: Estonia (Estonian Genome Center Biobank, University of Tartu), the Netherlands (LifeLines Cohort Study), Sweden (Swedish Twin Registry), and the United Kingdom (TwinsUK). Schizophrenia genetic risk for each woman in the AFB community sample was estimated using genetic effects inferred from the SCZ genome-wide association study. MAIN OUTCOMES AND MEASURES: We tested if SCZ genetic risk was a significant predictor of response variables based on published polynomial functions that described the relationship between maternal age and SCZ risk in offspring in Denmark. We substituted AFB for maternal age in these functions, one of which was corrected for the age of the father, and found that the fit was superior for the model without adjustment for the father's age. RESULTS: We observed a U-shaped relationship between SCZ risk and AFB in the community cohorts, consistent with the previously reported relationship between SCZ risk in offspring and maternal age when not adjusted for the age of the father. We confirmed that SCZ risk profile scores significantly predicted the response variables (coefficient of determination R2 = 1.1E-03, P = 4.1E-04), reflecting the published relationship between maternal age and SCZ risk in offspring by McGrath et al in 2014. CONCLUSIONS AND RELEVANCE: This study provides evidence for a significant overlap between genetic factors associated with risk of SCZ and genetic factors associated with AFB. It has been reported that SCZ risk associated with increased maternal age is explained by the age of the father and that de novo mutations that occur more frequently in the germline of older men are the underlying causal mechanism. This explanation may need to be revised if, as suggested herein and if replicated in future studies, there is also increased genetic risk of SCZ in older mothers.
IMPORTANCE: A recently published study of national data by McGrath et al in 2014 showed increased risk of schizophrenia (SCZ) in offspring associated with both early and delayed parental age, consistent with a U-shaped relationship. However, it remains unclear if the risk to the child is due to psychosocial factors associated with parental age or if those at higher risk for SCZ tend to have children at an earlier or later age. OBJECTIVE: To determine if there is a genetic association between SCZ and age at first birth (AFB) using genetically informative but independently ascertained data sets. DESIGN, SETTING, AND PARTICIPANTS: This investigation used multiple independent genome-wide association study data sets. The SCZ sample comprised 18 957 SCZ cases and 22 673 controls in a genome-wide association study from the second phase of the Psychiatric Genomics Consortium, and the AFB sample comprised 12 247 genotyped women measured for AFB from the following 4 community cohorts: Estonia (Estonian Genome Center Biobank, University of Tartu), the Netherlands (LifeLines Cohort Study), Sweden (Swedish Twin Registry), and the United Kingdom (TwinsUK). Schizophrenia genetic risk for each woman in the AFB community sample was estimated using genetic effects inferred from the SCZ genome-wide association study. MAIN OUTCOMES AND MEASURES: We tested if SCZ genetic risk was a significant predictor of response variables based on published polynomial functions that described the relationship between maternal age and SCZ risk in offspring in Denmark. We substituted AFB for maternal age in these functions, one of which was corrected for the age of the father, and found that the fit was superior for the model without adjustment for the father's age. RESULTS: We observed a U-shaped relationship between SCZ risk and AFB in the community cohorts, consistent with the previously reported relationship between SCZ risk in offspring and maternal age when not adjusted for the age of the father. We confirmed that SCZ risk profile scores significantly predicted the response variables (coefficient of determination R2 = 1.1E-03, P = 4.1E-04), reflecting the published relationship between maternal age and SCZ risk in offspring by McGrath et al in 2014. CONCLUSIONS AND RELEVANCE: This study provides evidence for a significant overlap between genetic factors associated with risk of SCZ and genetic factors associated with AFB. It has been reported that SCZ risk associated with increased maternal age is explained by the age of the father and that de novo mutations that occur more frequently in the germline of older men are the underlying causal mechanism. This explanation may need to be revised if, as suggested herein and if replicated in future studies, there is also increased genetic risk of SCZ in older mothers.
Authors: Brian M D'Onofrio; Martin E Rickert; Emma Frans; Ralf Kuja-Halkola; Catarina Almqvist; Arvid Sjölander; Henrik Larsson; Paul Lichtenstein Journal: JAMA Psychiatry Date: 2014-04 Impact factor: 21.596
Authors: L Felice Reddy; Junghee Lee; Michael C Davis; Lori Altshuler; David C Glahn; David J Miklowitz; Michael F Green Journal: Neuropsychopharmacology Date: 2013-08-21 Impact factor: 7.853
Authors: S Hong Lee; Stephan Ripke; Benjamin M Neale; Stephen V Faraone; Shaun M Purcell; Roy H Perlis; Bryan J Mowry; Anita Thapar; Michael E Goddard; John S Witte; Devin Absher; Ingrid Agartz; Huda Akil; Farooq Amin; Ole A Andreassen; Adebayo Anjorin; Richard Anney; Verneri Anttila; Dan E Arking; Philip Asherson; Maria H Azevedo; Lena Backlund; Judith A Badner; Anthony J Bailey; Tobias Banaschewski; Jack D Barchas; Michael R Barnes; Thomas B Barrett; Nicholas Bass; Agatino Battaglia; Michael Bauer; Mònica Bayés; Frank Bellivier; Sarah E Bergen; Wade Berrettini; Catalina Betancur; Thomas Bettecken; Joseph Biederman; Elisabeth B Binder; Donald W Black; Douglas H R Blackwood; Cinnamon S Bloss; Michael Boehnke; Dorret I Boomsma; Gerome Breen; René Breuer; Richard Bruggeman; Paul Cormican; Nancy G Buccola; Jan K Buitelaar; William E Bunney; Joseph D Buxbaum; William F Byerley; Enda M Byrne; Sian Caesar; Wiepke Cahn; Rita M Cantor; Miguel Casas; Aravinda Chakravarti; Kimberly Chambert; Khalid Choudhury; 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Bernie Devlin; John R Kelsoe; Pamela Sklar; Mark J Daly; Michael C O'Donovan; Nicholas Craddock; Patrick F Sullivan; Jordan W Smoller; Kenneth S Kendler; Naomi R Wray Journal: Nat Genet Date: 2013-08-11 Impact factor: 38.330
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Authors: D Paksarian; B B Trabjerg; K R Merikangas; O Mors; A D Børglum; D M Hougaard; J J McGrath; C B Pedersen; P B Mortensen; E Agerbo Journal: Psychol Med Date: 2017-06-29 Impact factor: 7.723
Authors: Gisela Sugranyes; Elena de la Serna; Roger Borras; Vanessa Sanchez-Gistau; Jose C Pariente; Soledad Romero; Inmaculada Baeza; Covadonga M Díaz-Caneja; Elisa Rodriguez-Toscano; Carmen Moreno; Miguel Bernardo; Dolores Moreno; Eduard Vieta; Josefina Castro-Fornieles Journal: Schizophr Bull Date: 2017-10-21 Impact factor: 9.306
Authors: Jacob Gratten; Naomi R Wray; Wouter J Peyrot; John J McGrath; Peter M Visscher; Michael E Goddard Journal: Nat Genet Date: 2016-05-23 Impact factor: 38.330
Authors: Nicola Barban; Rick Jansen; Ronald de Vlaming; Ahmad Vaez; Jornt J Mandemakers; Felix C Tropf; Xia Shen; James F Wilson; Daniel I Chasman; Ilja M Nolte; Vinicius Tragante; Sander W van der Laan; John R B Perry; Augustine Kong; Tarunveer S Ahluwalia; Eva Albrecht; Laura Yerges-Armstrong; Gil Atzmon; Kirsi Auro; Kristin Ayers; Andrew Bakshi; Danny Ben-Avraham; Klaus Berger; Aviv Bergman; Lars Bertram; Lawrence F Bielak; Gyda Bjornsdottir; Marc Jan Bonder; Linda Broer; Minh Bui; Caterina Barbieri; Alana Cavadino; Jorge E Chavarro; Constance Turman; Maria Pina Concas; Heather J Cordell; Gail Davies; Peter Eibich; Nicholas Eriksson; Tõnu Esko; Joel Eriksson; Fahimeh Falahi; Janine F Felix; Mark Alan Fontana; Lude Franke; Ilaria Gandin; Audrey J Gaskins; Christian Gieger; Erica P Gunderson; Xiuqing Guo; Caroline Hayward; Chunyan He; Edith Hofer; Hongyan Huang; Peter K Joshi; Stavroula Kanoni; Robert Karlsson; Stefan Kiechl; Annette Kifley; Alexander Kluttig; Peter Kraft; Vasiliki Lagou; Cecile Lecoeur; Jari Lahti; Ruifang Li-Gao; Penelope A Lind; Tian Liu; Enes Makalic; Crysovalanto Mamasoula; Lindsay Matteson; Hamdi Mbarek; Patrick F McArdle; George McMahon; S Fleur W Meddens; Evelin Mihailov; Mike Miller; Stacey A Missmer; Claire Monnereau; Peter J van der Most; Ronny Myhre; Mike A Nalls; Teresa Nutile; Ioanna Panagiota Kalafati; Eleonora Porcu; Inga Prokopenko; Kumar B Rajan; Janet Rich-Edwards; Cornelius A Rietveld; Antonietta Robino; Lynda M Rose; Rico Rueedi; Kathleen A Ryan; Yasaman Saba; Daniel Schmidt; Jennifer A Smith; Lisette Stolk; Elizabeth Streeten; Anke Tönjes; Gudmar Thorleifsson; Sheila Ulivi; Juho Wedenoja; Juergen Wellmann; Peter Willeit; Jie Yao; Loic Yengo; Jing Hua Zhao; Wei Zhao; Daria V Zhernakova; Najaf Amin; Howard Andrews; Beverley Balkau; Nir Barzilai; Sven Bergmann; Ginevra Biino; Hans Bisgaard; Klaus Bønnelykke; Dorret I Boomsma; Julie E Buring; Harry Campbell; Stefania Cappellani; Marina Ciullo; Simon R Cox; Francesco Cucca; Daniela Toniolo; George Davey-Smith; Ian J Deary; George Dedoussis; Panos Deloukas; Cornelia M van Duijn; Eco J C de Geus; Johan G Eriksson; Denis A Evans; Jessica D Faul; Cinzia Felicita Sala; Philippe Froguel; Paolo Gasparini; Giorgia Girotto; Hans-Jörgen Grabe; Karin Halina Greiser; Patrick J F Groenen; Hugoline G de Haan; Johannes Haerting; Tamara B Harris; Andrew C Heath; Kauko Heikkilä; Albert Hofman; Georg Homuth; Elizabeth G Holliday; John Hopper; Elina Hyppönen; Bo Jacobsson; Vincent W V Jaddoe; Magnus Johannesson; Astanand Jugessur; Mika Kähönen; Eero Kajantie; Sharon L R Kardia; Bernard Keavney; Ivana Kolcic; Päivikki Koponen; Peter Kovacs; Florian Kronenberg; Zoltan Kutalik; Martina La Bianca; Genevieve Lachance; William G Iacono; Sandra Lai; Terho Lehtimäki; David C Liewald; Cecilia M Lindgren; Yongmei Liu; Robert Luben; Michael Lucht; Riitta Luoto; Per Magnus; Patrik K E Magnusson; Nicholas G Martin; Matt McGue; Ruth McQuillan; Sarah E Medland; Christa Meisinger; Dan Mellström; Andres Metspalu; Michela Traglia; Lili Milani; Paul Mitchell; Grant W Montgomery; Dennis Mook-Kanamori; Renée de Mutsert; Ellen A Nohr; Claes Ohlsson; Jørn Olsen; Ken K Ong; Lavinia Paternoster; Alison Pattie; Brenda W J H Penninx; Markus Perola; Patricia A Peyser; Mario Pirastu; Ozren Polasek; Chris Power; Jaakko Kaprio; Leslie J Raffel; Katri Räikkönen; Olli Raitakari; Paul M Ridker; Susan M Ring; Kathryn Roll; Igor Rudan; Daniela Ruggiero; Dan Rujescu; Veikko Salomaa; David Schlessinger; Helena Schmidt; Reinhold Schmidt; Nicole Schupf; Johannes Smit; Rossella Sorice; Tim D Spector; John M Starr; Doris Stöckl; Konstantin Strauch; Michael Stumvoll; Morris A Swertz; Unnur Thorsteinsdottir; A Roy Thurik; Nicholas J Timpson; Joyce Y Tung; André G Uitterlinden; Simona Vaccargiu; Jorma Viikari; Veronique Vitart; Henry Völzke; Peter Vollenweider; Dragana Vuckovic; Johannes Waage; Gert G Wagner; Jie Jin Wang; Nicholas J Wareham; David R Weir; Gonneke Willemsen; Johann Willeit; Alan F Wright; Krina T Zondervan; Kari Stefansson; Robert F Krueger; James J Lee; Daniel J Benjamin; David Cesarini; Philipp D Koellinger; Marcel den Hoed; Harold Snieder; Melinda C Mills Journal: Nat Genet Date: 2016-10-31 Impact factor: 38.330