Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-04T19:43:32.917Z Has data issue: false hasContentIssue false
  • English
  • Français

Advanced paternal age at birth: phenotypic and etiologic associations with eating pathology in offspring

Published online by Cambridge University Press:  24 June 2013

S. E. Racine ,
K. M. Culbert ,
S. A. Burt  and
K. L. Klump
S. E. Racine
Affiliation:
Department of Psychology, Michigan State University, East Lansing, MI, USA
K. M. Culbert
Affiliation:
Department of Psychiatry and Behavioral Neuroscience, University of Chicago, Chicago, IL, USA
S. A. Burt
Affiliation:
Department of Psychology, Michigan State University, East Lansing, MI, USA
K. L. Klump*
Affiliation:
Department of Psychology, Michigan State University, East Lansing, MI, USA
*
*Address for correspondence: K. L. Klump, Ph.D., Department of Psychology, Michigan State University, 316 Physics Road-107B, East Lansing, MI 48824-1116, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Advanced paternal age at birth has been linked to several psychiatric disorders in offspring (e.g. schizophrenia) and genetic mechanisms are thought to underlie these associations. This study is the first to investigate whether advanced paternal age at birth is associated with eating disorder risk using a twin study design capable of examining both phenotypic and genetic associations.

Method

In a large, population-based sample of female twins aged 8–17 years in mid-puberty or beyond (n = 1722), we investigated whether advanced paternal age was positively associated with disordered eating symptoms and an eating disorder history [i.e. anorexia nervosa (AN), bulimia nervosa (BN) or binge eating disorder (BED)] in offspring. Biometric twin models examined whether genetic and/or environmental factors underlie paternal age effects for disordered eating symptoms.

Results

Advanced paternal age was positively associated with disordered eating symptoms and an eating disorder history, where the highest level of pathology was observed in offspring born to fathers ⩾40 years old. The results were not accounted for by maternal age at birth, body mass index (BMI), socio-economic status (SES), fertility treatment or parental psychiatric history. Twin models indicated decreased genetic, and increased environmental, effects on disordered eating with advanced paternal age.

Conclusions

Advanced paternal age increased risk for the full spectrum of eating pathology, independent of several important covariates. However, contrary to leading hypotheses, environmental rather than genetic factors accounted for paternal age–disordered eating associations. These data highlight the need to explore novel (potentially environmental) mechanisms underlying the effects of advanced paternal age on offspring eating disorder risk.

Keywords

Advanced paternal agedisordered eatingeating disordersenvironmentalgenetictwin study
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 5 , April 2014 , pp. 1029 - 1041
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Parts of this paper were presented at the Eating Disorders Research Society meeting, Edinburgh, Scotland, UK, 22–24 September 2011.

References

Agrawal, A, Balasubramanian, S, Smith, EK, Madden, PA, Bucholz, KK, Heath, AC, Lynskey, MT (2010). Peer substance involvement modifies genetic influences on regular substance involvement in young women. Addiction 105, 1844–1853.Google Scholar
APA (2000). Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision. American Psychiatric Association: Washington, DC.Google Scholar
Awadalla, P, Gauthier, J, Myers, RA, Casals, F, Hamdan, FF, Griffing, AR, Côté, M, Henrion, E, Spiegelman, D, Tarabeux, J, Piton, A, Yang, Y, Boyko, A, Bustamante, C, Xiong, L, Rapoport, JL, Addington, AM, DeLisi, JLE, Krebs, M, Joober, R, Millet, B, Fombonne, E, Mottron, L, Zilversmit, M, Keebler, J, Daoud, H, Marineau, C, Roy-Gagnon, M, Dube, M, Eyre-Walker, A, Drapeau, P, Stone, EA, Lafreniere, RG, Rouleau, GA (2010). Direct measure of the de novo mutation rate in autism and schizophrenia cohorts. American Journal of Human Genetics 87, 316–324.Google Scholar
Burt, SA, Klump, KL (2013). The Michigan State University Twin Registry: an update. Twin Research and Human Genetics 16, 344–350.Google Scholar
Byrne, M, Agerbo, E, Ewald, H, Eaton, WW, Mortensen, PB (2003). Parental age and risk of schizophrenia: a case-control study. Archives of General Psychiatry 60, 673–678.Google Scholar
Cannon, M, Jones, PB, Murray, RM (2002). Obstetric complications and schizophrenia: historical and meta-analytic review. American Journal of Psychiatry 159, 1080–1092.Google Scholar
Croen, LA, Najjar, DV, Fireman, B, Grether, JK (2007). Maternal and paternal age and risk of autism spectrum disorders. Archives of Pediatrics and Adolescent Medicine 161, 334–340.Google Scholar
Croll, J, Neumark-Sztainer, D, Story, M, Ireland, M (2002). Prevalence and risk and protective factors related to disordered eating behaviors among adolescents: relationship to gender and ethnicity. Journal of Adolescent Health 31, 166–175.CrossRefGoogle ScholarPubMed
Crow, JF (2000). The origins, patterns and implications of human spontaneous mutation. Nature Reviews Genetics 1, 40–47.Google Scholar
Culbert, KM, Burt, SA, McGue, M, Iacono, WG, Klump, KL (2009). Puberty and the genetic diathesis of disordered eating attitudes and behaviors. Journal of Abnormal Psychology 118, 788–796.Google Scholar
Doornbos, ME, Maas, SM, McDonnell, J, Vermeiden, JPW, Hennekam, RCM (2007). Infertility, assisted reproduction technologies and imprinting disturbances: a Dutch study. Human Reproduction 22, 2476–2480.Google Scholar
Eriksen, W, Sundet, JM, Tambs, K (2012). Paternal age at birth and the risk of obesity in young adulthood: a register-based birth cohort study of Norwegian males. American Journal of Human Biology 25, 29–34.Google Scholar
Fairburn, CG, Beglin, SJ (1994). Assessment of eating disorders: interview or self-report questionnaire? International Journal of Eating Disorders 16, 363–370.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Favaro, A, Tenconi, E, Santonastaso, P (2006). Perinatal factors and the risk of developing anorexia nervosa and bulimia nervosa. Archives of General Psychiatry 63, 82–88.CrossRefGoogle ScholarPubMed
Frans, EM, Sandin, S, Reichenberg, A, Lichtenstein, P, Langstrom, N, Hultman, CM (2008). Advancing paternal age and bipolar disorder. Archives of General Psychiatry 65, 1034–1040.Google Scholar
Frieling, H, Römer, KD, Scholz, S, Mittelbach, F, Wilhelm, J, De Zwaan, M, Jacoby, GE, Kornhuber, J, Hillemacher, T, Bleich, S (2010). Epigenetic dysregulation of dopaminergic genes in eating disorders. International Journal of Eating Disorders 43, 577–583.Google Scholar
Gagne, DA, Von Holle, A, Brownley, KA, Runfola, CD, Hofmeier, S, Branch, KE, Bulik, CM (2012). Eating disorder symptoms and weight and shape concerns in a large web-based convenience sample of women ages 50 and above: results of the gender and body image (GABI) study. International Journal of Eating Disorders 45, 832–844.Google Scholar
Hare, E, Moran, P (1979). Raised parental age in psychiatric patients: evidence for the constitutional hypothesis. British Journal of Psychiatry 134, 169–177.Google Scholar
Harlap, S, Paltiel, O, Deutsch, L, Knaanie, A, Masalha, S, Tiram, E, Caplan, LS, Malaspina, D, Friedlander, Y (2002). Paternal age and preeclampsia. Epidemiology 13, 660–667.Google Scholar
Hultman, C, Sandin, S, Levine, S, Lichtenstein, P, Reichenberg, A (2011). Advancing paternal age and risk of autism: new evidence from a population-based study and a meta-analysis of epidemiological studies. Molecular Psychiatry 16, 1203–1212.Google Scholar
Huybrechts, I, Himes, JH, Ottevaere, C, De Vriendt, T, De Keyzer, W, Cox, B, Van Trimpont, I, De Bacquer, D, De Henauw, S (2011). Validity of parent-reported weight and height of preschool children measured at home or estimated without home measurement: a validation study. BMC Pediatrics 11, 63.Google Scholar
Insel, TR, Cuthbert, BN, Garvey, MA, Heinssen, RK, Pine, DS, Quinn, KJ, Sanislow, CA, Wang, PS (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. American Journal of Psychiatry 167, 748–751.Google Scholar
Iossifov, I, Ronemus, M, Levy, D, Wang, Z, Hakker, I, Rosenbaum, J, Yamrom, B, Lee, Y, Narzisi, G, Leotta, A, Kendall, J, Grabowska, E, Ma, B, Marks, S, Rodgers, L, Stepansky, A, Troge, J, Andrews, P, Bekritsky, M, Pradhan, K, Ghiban, E, Kramer, M, Parla, J, Demeter, R, Fulton, LL, Fulton, RS, Magrini, VJ, Ye, K, Darnell, JC, Darnell, RB, Mardis, ER, Wilson, RK, Schatz, MC, McCombie, WR, Wigler, M (2012). De novo gene disruptions in children on the autistic spectrum. Neuron 74, 285–299.Google Scholar
Jacobi, C, Hayward, C, de Zwaan, M, Kraemer, HC, Agras, WS (2004). Coming to terms with risk factors for eating disorders: application of risk terminology and suggestions for a general taxonomy. Psychological Bulletin 130, 19–65.Google Scholar
Kaminsky, ZA, Tang, T, Wang, SC, Ptak, C, Oh, GHT, Wong, AHC, Feldcamp, LA, Virtanen, C, Halfvarson, J, Tysk, C, McRae, AF, Visscher, PM, Montgomery, GW, Gottesman, II, Martin, NG, Petronis, A (2009). DNA methylation profiles in monozygotic and dizygotic twins. Nature Genetics 41, 240–245.Google Scholar
Keel, PK, Baxter, MG, Heatherton, TF, Joiner, TE (2007). A 20-year longitudinal study of body weight, dieting, and eating disorder symptoms. Journal of Abnormal Psychology 116, 422–432.Google Scholar
Kendler, KS, Heath, AC, Neale, MC, Kessler, RC, Eaves, LJ (1992). A population-based twin study of alcoholism in women. Journal of the American Medical Association 268, 1877–1882.Google Scholar
Killen, J, Hayward, C, Litt, I, Hammer, L, Wilson, D, Miner, B, Taylor, C, Varady, A, Shisslak, C (1992). Is puberty a risk factor for eating disorders? Archives of Pediatrics and Adolescent Medicine 146, 323–325.Google Scholar
Klump, KL, Bulik, CM, Kaye, WH, Treasure, J, Tyson, E (2009). Academy for eating disorders position paper: eating disorders are serious mental illnesses. International Journal of Eating Disorders 42, 97–103.Google Scholar
Klump, KL, Burt, SA (2006). The Michigan State University Twin Registry (MSUTR): genetic, environmental and neurobiological influences on behavior across development. Twin Research and Human Genetics 9, 971–977.Google Scholar
Klump, KL, Keel, PK, Racine, SE, Burt, SA, Neale, M, Sisk, C, Boker, S, Hu, JY (2013). The interactive effects of estrogen and progesterone on changes in emotional eating across the menstrual cycle. Journal of Abnormal Psychology 122, 131–137.CrossRefGoogle ScholarPubMed
Klump, KL, Keel, PK, Sisk, C, Burt, SA (2010). Preliminary evidence that estradiol moderates genetic influences on disordered eating attitudes and behaviors during puberty. Psychological Medicine 40, 1745–1753.Google Scholar
Klump, KL, Perkins, PS, Alexandra Burt, S, McGue, M, Iacono, WG (2007). Puberty moderates genetic influences on disordered eating. Psychological Medicine 37, 627–634.Google Scholar
Kolko, DJ, Kazdin, AE (1993). Emotional/behavioral problems in clinic and nonclinic children: correspondence among child, parent and teacher reports. Journal of Child Psychology and Psychiatry 34, 991–1006.Google Scholar
Kong, A, Frigge, ML, Masson, G, Besenbacher, S, Sulem, P, Magnusson, G, Gudjonsson, SA, Sigurdsson, A, Jonasdottir, A, Jonasdottir, A, Wong, WSW, Sigurdsson, G, Walters, GB, Steinberg, S, Helgason, H, Thorleifsson, G, Gudbjartsson, DF, Helgason, A, Magnusson, OT, Thorsteinsdottir, U, Stefansson, K (2012). Rate of de novo mutations and the importance of father's age to disease risk. Nature 488, 471–475.Google Scholar
Lewinsohn, PM, Striegel-Moore, RH, Seeley, JR (2000). Epidemiology and natural course of eating disorders in young women from adolescence to young adulthood. Journal of the American Academy of Child and Adolescent Psychiatry 39, 1284–1292.Google Scholar
Lichtenstein, P (2002). The Swedish Twin Registry: a unique resource for clinical, epidemiological and genetic studies. Journal of Internal Medicine 252, 184–205.Google Scholar
Lilenfeld, LR, Kaye, WH, Greeno, CG, Merikangas, KR, Plotnicov, K, Pollice, C, Rao, R, Strober, M, Bulik, CM, Nagy, L (1998). A controlled family study of anorexia nervosa and bulimia nervosa: psychiatric disorders in first-degree relatives and effects of proband comorbidity. Archives of General Psychiatry 55, 603–610.Google Scholar
Liu, K, Zerubavel, N, Bearman, P (2010). Social demographic change and autism. Demography 47, 327–343.CrossRefGoogle ScholarPubMed
Lundström, S, Haworth, C, Carlström, E, Gillberg, C, Mill, J, Råstam, M, Hultman, CM, Ronald, A, Anckarsäter, H, Plomin, R, Lichtenstein, P, Reichenberg, A (2010). Trajectories leading to autism spectrum disorders are affected by paternal age: findings from two nationally representative twin studies. Journal of Child Psychology and Psychiatry 51, 850–856.CrossRefGoogle ScholarPubMed
Lykken, D, Bouchard, T, McGue, M, Tellegen, A (1990). The Minnesota Twin Family Registry. Acta Geneticae Medicae et Gemellologiae 39, 35–70.Google Scholar
Malaspina, D, Corcoran, C, Fahim, C, Berman, A, Harkave-Friedman, J, Yale, S, Goetz, D, Goetz, R, Harlap, S, Gorman, J (2002). Paternal age and sporadic schizophrenia: evidence for de novo mutations. American Journal of Medical Genetics 114, 299–303.Google Scholar
Malaspina, D, Harlap, S, Fennig, S, Heiman, D, Nahon, D, Feldman, D, Susser, ES (2001). Advancing paternal age and the risk of schizophrenia. Archives of General Psychiatry 58, 361–367.Google Scholar
Maloney, MJ, McGuire, J, Daniels, SR, Specker, B (1989). Dieting behavior and eating attitudes in children. Pediatrics 84, 482–489.Google Scholar
Menezes, P, Lewis, G, Rasmussen, F, Zammit, S, Sipos, A, Harrison, G, Tynelius, P, Gunnell, D (2010). Paternal and maternal ages at conception and risk of bipolar affective disorder in their offspring. Psychological Medicine 40, 477–485.Google Scholar
Merikangas, KR, He, JP, Brody, D, Fisher, PW, Bourdon, K, Koretz, DS (2010). Prevalence and treatment of mental disorders among US children in the 2001–2004 NHANES. Pediatrics 125, 75–81.Google Scholar
Miller, B, Messias, E, Miettunen, J, Alaräisänen, A, Järvelin, MR, Koponen, H, Räsänen, P, Isohanni, M, Kirkpatrick, B (2011). Meta-analysis of paternal age and schizophrenia risk in male versus female offspring. Schizophrenia Bulletin 37, 1039–1047.Google Scholar
Neale, MC (1997). Mx: Statistical Modeling, 4th edn. Department of Psychiatry, Medical College of Virginia: Richmond, VA.Google Scholar
Neale, MC, Aggen, SH, Maes, HH, Kubarych, TS, Schmitt, JE (2006). Methodological issues in the assessment of substance use phenotypes. Addictive Behaviors 31, 1010–1034.Google Scholar
O'Dea, JA, Caputi, P (2001). Association between socioeconomic status, weight, age and gender, and the body image and weight control practices of 6- to 19-year-old children and adolescents. Health Education Research 16, 521–532.Google Scholar
Perrin, MC, Brown, AS, Malaspina, D (2007). Aberrant epigenetic regulation could explain the relationship of paternal age to schizophrenia. Schizophrenia Bulletin 33, 1270–1273.CrossRefGoogle ScholarPubMed
Petersen, AC, Crockett, L, Richards, M, Boxer, A (1988). A self-report measure of pubertal status: reliability, validity, and initial norms. Journal of Youth and Adolescence 17, 117–133.Google Scholar
Purcell, S (2002). Variance components models for gene-environment interaction in twin analysis. Twin Research 5, 554–571.Google Scholar
Reichenberg, A, Gross, R, Weiser, M, Bresnahan, M, Silverman, J, Harlap, S, Rabinowitz, J, Shulman, C, Malaspina, D, Lubin, G, Knobler, HY, Davidson, M, Susser, E (2006). Advancing paternal age and autism. Archives of General Psychiatry 63, 1026–1032.Google Scholar
Ronald, A, Hoekstra, RA (2011). Autism spectrum disorders and autistic traits: a decade of new twin studies. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics 156, 255–274.Google Scholar
Sartorius, GA, Nieschlag, E (2010). Paternal age and reproduction. Human Reproduction Update 16, 65–79.Google Scholar
Schanen, NC (2006). Epigenetics of autism spectrum disorders. Human Molecular Genetics 15, R138–R150.Google Scholar
Shah, PS (2010). Paternal factors and low birthweight, preterm, and small for gestational age births: a systematic review. American Journal of Obstetrics and Gynecology 202, 103–123.Google Scholar
Sobotka, T (2010). Shifting parenthood to advanced reproductive ages: trends, causes and consequences. In A Young Generation Under Pressure? (ed. Tremmel, J. C.), pp. 129–154. Springer: New York.Google Scholar
Steinglass, JE, Eisen, JL, Attia, E, Mayer, L, Walsh, BT (2007). Is anorexia nervosa a delusional disorder? An assessment of eating beliefs in anorexia nervosa. Journal of Psychiatric Practice 13, 65–71.Google Scholar
Swanson, SA, Crow, SJ, Le Grange, D, Swendsen, J, Merikangas, KR (2011). Prevalence and correlates of eating disorders in adolescents: results from the national comorbidity survey replication adolescent supplement. Archives of General Psychiatry 68, 714–723.Google Scholar
Tang, CH, Wu, MP, Liu, JT, Lin, HC, Hsu, CC (2006). Delayed parenthood and the risk of cesarean delivery – is paternal age an independent risk factor? Birth 33, 18–26.Google Scholar
Wade, TD, Byrne, S, Bryant-Waugh, R (2008). The Eating Disorder Examination: norms and construct validity with young and middle adolescent girls. International Journal of Eating Disorders 41, 551–558.Google Scholar
Wohl, M, Gorwood, P (2007). Paternal ages below or above 35 years old are associated with a different risk of schizophrenia in the offspring. European Psychiatry 22, 22–26.Google Scholar
Xu, B, Roos, JL, Dexheimer, P, Boone, B, Plummer, B, Levy, S, Gogos, JA, Karayiorgou, M (2011). Exome sequencing supports a de novo mutational paradigm for schizophrenia. Nature Genetics 43, 864–868.Google Scholar
Youngstrom, E, Loeber, R, Stouthamer-Loeber, M (2000). Patterns and correlates of agreement between parent, teacher, and male adolescent ratings of externalizing and internalizing problems. Journal of Consulting and Clinical Psychology 68, 1038–1050.Google Scholar
Zhao, X, Leotta, A, Kustanovich, V, Lajonchere, C, Geschwind, DH, Law, K, Law, P, Qiu, S, Lord, C, Sebat, J, Ye, K, Wigler, M (2007). A unified genetic theory for sporadic and inherited autism. Proceedings of the National Academy of Sciences USA 104, 12 831–12 836.Google Scholar
Zucker, NL, Losh, M, Bulik, CM, LaBar, KS, Piven, J, Pelphrey, KA (2007). Anorexia nervosa and autism spectrum disorders: guided investigation of social cognitive endophenotypes. Psychological Bullentin 133, 976–1006.Google Scholar