Intolerance of loud sounds in childhood: Is there an intergenerational association with grandmaternal smoking in pregnancy?

Recent research using the Avon Longitudinal Study of Parents and Children (ALSPAC) demonstrated an association between maternal grandmother smoking in pregnancy and the autistic traits of impaired social communication and repetitive behaviour in granddaughters but not grandsons, but of paternal grandmother smoking and early development of myopia in the grandchild. Here we investigate whether grandmaternal smoking in pregnancy is associated with intolerance to loud sounds. ALSPAC collected information during the index pregnancy from the study parents on the smoking habits, social and other features of their own parents. Maternal report when the child was aged 6 and 13 included hating loud sounds; at age 11 the child was tested for volume preference for listening to music through headphones. Statistical analysis compared results for grandchildren in relation to whether a parent had been exposed in utero to maternal smoking, adjusted for their grandparents’ social and demographic attributes. We hypothesised that there would be sex differences in the effects of grandmaternal prenatal smoking, based on previous intergenerational studies. For 6-year-old children maternal report of intolerance to loud noise was more likely in grandsons if the maternal grandmother had smoked [adjusted odds ratio (AOR) 1.27; 95% confidence interval (CI) 1.03,1.56; P = 0.025], but less likely in girls [AOR 0.82; 95%CI 0.63,1.07] Pinteraction <0.05. If the paternal grandmother had smoked the grandchildren were less likely to be intolerant, especially girls. The objective measure of choice of volume for music through headphones showed that grandsons of both maternal and paternal smoking grandmothers were less likely to choose high volumes compared with granddaughters (P<0.05). In line with our prior hypothesis of sex differences, we showed that grandsons were more intolerant of loud sounds than granddaughters particularly at age 6, and this was confirmed by objective measures at age 11.

[1]  M. Pembrey,et al.  Grandmothers’ smoking in pregnancy is associated with a reduced prevalence of early-onset myopia , 2019, Scientific Reports.

[2]  E. Manias,et al.  Improving medication adherence in adult kidney transplantation (IMAKT): A pilot randomised controlled trial , 2019, Scientific reports.

[3]  G. D. da Rocha,et al.  Occurrence of the potent mutagens 2- nitrobenzanthrone and 3-nitrobenzanthrone in fine airborne particles , 2019, Scientific Reports.

[4]  B. Stranger,et al.  The role of sex in the genomics of human complex traits , 2018, Nature Reviews Genetics.

[5]  Pia R. Pinger,et al.  Paternal grandfather’s access to food predicts all-cause and cancer mortality in grandsons , 2018, Nature Communications.

[6]  Veronika A. Herzog,et al.  Small RNAs are trafficked from the epididymis to developing mammalian sperm , 2017, bioRxiv.

[7]  G. Grant,et al.  Transgenerational inheritance of chronic adolescent stress: Effects of stress response and the amygdala transcriptome , 2018, Genes, brain, and behavior.

[8]  Karim Mekhail.  Corrigendum: Defining the Damaged DNA Mobility Paradox as Revealed by the Study of Telomeres, DSBs, Microtubules and Motors , 2018, Front. Genet..

[9]  M. Skinner,et al.  Environmentally induced epigenetic transgenerational inheritance of disease , 2018, Environmental epigenetics.

[10]  Karim Mekhail.  Defining the Damaged DNA Mobility Paradox as Revealed by the Study of Telomeres, DSBs, Microtubules and Motors , 2018, Front. Genet..

[11]  B. Forsberg,et al.  Grandmaternal smoking increases asthma risk in grandchildren: A nationwide Swedish cohort , 2018, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[12]  K. Birmingham.  Pioneering Ethics in a Longitudinal Study , 2018 .

[13]  P. Vineis,et al.  Epigenetic supersimilarity of monozygotic twin pairs , 2018, Genome Biology.

[14]  A. Nielsen,et al.  DNA methylation in epigenetic inheritance of metabolic diseases through the male germ line. , 2017, Journal of molecular endocrinology.

[15]  D. Posthuma,et al.  Majority of human traits do not show evidence for sex-specific genetic and environmental effects , 2017, Scientific Reports.

[16]  J. Guinan,et al.  Efferent inhibition strength is a physiological correlate of hyperacusis in children with autism spectrum disorder. , 2017, Journal of neurophysiology.

[17]  Yang I Li,et al.  An Expanded View of Complex Traits: From Polygenic to Omnigenic , 2017, Cell.

[18]  M. Pembrey,et al.  Grand-maternal smoking in pregnancy and grandchild’s autistic traits and diagnosed autism , 2017, Scientific Reports.

[19]  C. Brewer,et al.  Auditory Phenotype of Smith-Magenis Syndrome. , 2017, Journal of speech, language, and hearing research : JSLHR.

[20]  A. Sharma.  Transgenerational epigenetics: Integrating soma to germline communication with gametic inheritance , 2017, Mechanisms of Ageing and Development.

[21]  Marcelo P. Segura-Lepe,et al.  Rare and low-frequency coding variants alter human adult height , 2016, Nature.

[22]  Pia R. Pinger,et al.  Transgenerational Effects of Childhood Conditions on Third Generation Health and Education Outcomes , 2014, Economics and human biology.

[23]  E. Miska,et al.  Transgenerational inheritance: Models and mechanisms of non–DNA sequence–based inheritance , 2016, Science.

[24]  Hsiu-Hsi Chen,et al.  Longer Duration and Earlier Age of Onset of Paternal Betel Chewing and Smoking Increase Metabolic Syndrome Risk in Human Offspring, Independently, in a Community-Based Screening Program in Taiwan , 2016, Circulation.

[25]  S. Rich.  Diabetes: Still a geneticist's nightmare , 2016, Nature.

[26]  Stephen C. J. Parker,et al.  The genetic architecture of type 2 diabetes , 2016, Nature.

[27]  T. Bourgeron,et al.  CNTN6 mutations are risk factors for abnormal auditory sensory perception in autism spectrum disorders , 2016, Molecular Psychiatry.

[28]  I. Mansuy,et al.  Molecular insights into transgenerational non-genetic inheritance of acquired behaviours , 2015, Nature Reviews Genetics.

[29]  D. Wolfer,et al.  Early life stress in fathers improves behavioural flexibility in their offspring , 2014, Nature Communications.

[30]  R. Salvi,et al.  Central Gain Control in Tinnitus and Hyperacusis , 2014, Front. Neurol..

[31]  J. Peña-Diaz,et al.  The dual nature of mismatch repair as antimutator and mutator: for better or for worse , 2014, Front. Genet..

[32]  M. Pembrey,et al.  The anthropometry of children and adolescents may be influenced by the prenatal smoking habits of their grandmothers: A longitudinal cohort study , 2014, American journal of human biology : the official journal of the Human Biology Council.

[33]  M. Pembrey,et al.  Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research , 2014, Journal of Medical Genetics.

[34]  L. Farinelli,et al.  Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice , 2014, Nature Neuroscience.

[35]  M. Pembrey,et al.  Prepubertal start of father's smoking and increased body fat in his sons: further characterisation of paternal transgenerational responses , 2014, European Journal of Human Genetics.

[36]  M. Pembrey,et al.  Is the Growth of the Fetus of a Non-Smoking Mother Influenced by the Smoking of Either Grandmother while Pregnant? , 2014, PloS one.

[37]  L. Rüttiger,et al.  Advances in the neurobiology of hearing disorders: Recent developments regarding the basis of tinnitus and hyperacusis , 2013, Progress in Neurobiology.

[38]  M. Kas,et al.  Contactins in the neurobiology of autism. , 2013, European journal of pharmacology.

[39]  L. Feig,et al.  Chronic Social Instability Induces Anxiety and Defective Social Interactions Across Generations , 2013, Biological Psychiatry.

[40]  F. Champagne.  Effects of Stress Across Generations: Why Sex Matters , 2013, Biological Psychiatry.

[41]  G. Brunborg,et al.  Cigarette smoke‐induced transgenerational alterations in genome stability in cord blood of human F1 offspring , 2012, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[42]  D. Lawlor,et al.  Cohort Profile: The Avon Longitudinal Study of Parents and Children: ALSPAC mothers cohort , 2012, International journal of epidemiology.

[43]  D. Lawlor,et al.  Cohort Profile: The ‘Children of the 90s’—the index offspring of the Avon Longitudinal Study of Parents and Children , 2012, International journal of epidemiology.

[44]  A. Karmiloff-Smith,et al.  Severity of hyperacusis predicts individual differences in speech perception in Williams Syndrome. , 2011, Journal of intellectual disability research : JIDR.

[45]  T. Bale,et al.  Maternal high-fat diet effects on third-generation female body size via the paternal lineage. , 2011, Endocrinology.

[46]  M. Pembrey.  Male-line transgenerational responses in humans , 2010, Human fertility.

[47]  H. Putter,et al.  DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. , 2009, Human molecular genetics.

[48]  Philip X. Joris,et al.  Recruitment of Neurons and Loudness , 2009, Journal of the Association for Research in Otolaryngology.

[49]  M. Wagner,et al.  Auditory hypersensitivity in the autistic spectrum disorder. , 2008, Pro-fono : revista de atualizacao cientifica.

[50]  Kent L Thornburg,et al.  Effect of in Utero and Early-life Conditions on Adult Health and Disease Epidemiol Ogic a Nd Clinic a L Observations , 2022 .

[51]  Simon C. Potter,et al.  Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls , 2007, Nature.

[52]  W. Alvord,et al.  Preconceptional fasting of fathers alters serum glucose in offspring of mice. , 2006, Nutrition.

[53]  M. Pembrey,et al.  Sex-specific, male-line transgenerational responses in humans , 2006, European Journal of Human Genetics.

[54]  J. Golding.  The Avon Longitudinal Study of Parents and Children (ALSPAC)--study design and collaborative opportunities. , 2004, European journal of endocrinology.

[55]  A. Petronis.  The origin of schizophrenia: genetic thesis, epigenetic antithesis, and resolving synthesis , 2004, Biological Psychiatry.

[56]  B. Tepper,et al.  A paper screening test to assess genetic taste sensitivity to 6-n-propylthiouracil , 2003, Physiology & Behavior.

[57]  S. Edvinsson,et al.  Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period , 2002, European Journal of Human Genetics.

[58]  S. Edvinsson,et al.  Longevity Determined by Paternal Ancestors' Nutrition during Their Slow Growth Period , 2001, Acta biotheoretica.

[59]  J. Barrett,et al.  Genomic imprinting and environmental disease susceptibility. , 2000, Environmental health perspectives.

[60]  U Rosenhall,et al.  Autism and Hearing Loss , 1999, Journal of autism and developmental disorders.

[61]  L. Lumey,et al.  Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 1944-1945. , 1992, Paediatric and perinatal epidemiology.

[62]  P. Bradley,et al.  Fetal and infant origins of adult disease. , 1991, BMJ.

[63]  B. Walker,et al.  The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. , 2004, The Journal of endocrinology.

[64]  B. Boucher,et al.  Betel nut (Areca catechu) consumption and the induction of glucose intolerance in adult CD1 mice and in their F1 and F2 offspring , 2004, Diabetologia.

[65]  M. Pembrey,et al.  ALSPAC--the Avon Longitudinal Study of Parents and Children. I. Study methodology. , 2001, Paediatric and perinatal epidemiology.