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Sex-Specific Serum Biomarker Patterns in Adults with Asperger's Syndrome

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Sex-Specific Serum Biomarker Patterns in Adults with Asperger's Syndrome Molecular Psychiatry (2010), 1–8 & 2010 Macmillan Publishers Limited All rights reserved 1359-4184/10 www.nature.com/mp ORIGINAL ARTICLE Sex-specific serum biomarker patterns in adults with Asperger’s syndrome E Schwarz1, PC Guest1, H Rahmoune1, L Wang1, Y Levin1, E Ingudomnukul2, L Ruta2,3, L Kent2,4, M Spain5, S Baron-Cohen2 and S Bahn1,6 1Institute of Biotechnology, University of Cambridge, Cambridge, UK; 2Department of Psychiatry, Autism Research Centre, University of Cambridge, Cambridge, UK; 3Division of Child Neurology and Psychiatry, Department of Pediatrics, University of Catania, Catania, Italy; 4Bute Medical School, University of St Andrews, Scotland, UK; 5Rule Based Medicine, Austin, TX, USA and 6Department of Neuroscience, Erasmus MC, Rotterdam, The Netherlands Autism spectrum conditions have been hypothesized to be an exaggeration of normal male low-empathizing and high-systemizing behaviors. We tested this hypothesis at the molecular level by performing comprehensive multi-analyte profiling of blood serum from adult subjects with Asperger’s syndrome (AS) compared with controls. This led to identification of distinct sex-specific biomarker fingerprints for male and female subjects. Males with AS showed altered levels of 24 biomarkers including increased levels of cytokines and other inflammatory molecules. Multivariate statistical classification of males using this panel of 24 biomarkers revealed a marked separation between AS and controls with a sensitivity of 0.86 and specificity of 0.88. Testing this same panel in females did not result in a separation between the AS and control groups. In contrast, AS females showed altered levels of 17 biomarkers including growth factors and hormones such as androgens, growth hormone and insulin-related molecules. Classification of females using this biomarker panel resulted in a separation between AS and controls with sensitivities and specificities of 0.96 and 0.83, respectively, and testing this same panel in the male group did not result in a separation between the AS and control groups. The finding of elevated testosterone in AS females confirmed predictions from the ‘extreme male brain’ and androgen theories of autism spectrum conditions. We conclude that to understand the etiology and development of autism spectrum conditions, stratification by sex is essential. Molecular Psychiatry advance online publication, 28 September 2010; doi:10.1038/mp.2010.102 Keywords: Asperger’s syndrome; serum; gender; sexual dimorphism; profiling; biomarker Introduction on tests of empathy and social sensitivity and show stronger interest in systems. People with autism Autism spectrum conditions are diagnosed on the spectrum conditions show an exaggeration of this basis of difficulties in communication and social cognitive profile, which has led to the ‘extreme male development, in addition to unusually narrow inter- brain’ (EMB) theory as an explanation of the psycho- ests, repetitive behavior and resistance to change.1 logical manifestations.5 The EMB theory is supported The two major subgroups are classic autism and by the finding of tomboyism and other masculine Asperger’s syndrome (AS). AS differs from classic behaviors in females with autism spectrum condi- autism in that there is no history of language delay tions.6 The EMB theory has been extended recently or learning difficulties.2 The prevalence of autism to the neurological level. For example, in typical spectrum conditions is 1% of the general population3 males the overall brain volume and specific regions and there is a marked sex difference, with males being such as the amygdala are larger. In autism spectrum 4–10 times more likely to be affected than females.4 conditions, these differences are even more extreme.7 This suggests that sex-linked factors might have a However, little is known about the molecular path- role in the etiology of the condition. In the general ways underlying these effects. population, males on average perform at lower levels The fetal androgen theory of autism spectrum conditions7 suggests that increased levels of fetal Correspondence: Professor S Baron-Cohen, Department of Psychi- testosterone leads to typical sex differences in brain atry, Autism Research Centre, University of Cambridge, Cambridge structure and function. Individual differences in CB2 8AH, UK or Dr S Bahn, Institute of Biotechnology, University amniotic fetal testosterone are positively correlated of Cambridge, Tennis Court Road, Cambridge CB2 1QT, UK. 8 9 E-mail: [email protected] or [email protected] with number of autistic traits and systemizing, and Received 22 September 2009; revised 2 August 2010; accepted 8 negatively correlated with language development, August 2010 social development and empathy.10 This theory is Sex-specific biomarkers in Asperger’s syndrome E Schwarz et al 2 also supported by the observation of an increased rate Manual-IV-Text Review Disorders and accepted inter- of testosterone-related disorders such as polycystic national criteria (DSM-IV-TR). The Wechsler Abbre- ovary syndrome, acne and hirsutism in women with viated Scale of Intelligence was administered to autism spectrum conditions,11 a lower ratio of the all participants to measure intelligence quotient. second (index) and fourth (ring) digit lengths (2D:4D) All diagnoses and clinical tests were performed in both males and females with autism spectrum by psychiatrists under Good Clinical Practice conditions,12 and an association of autism spectrum compliance to minimize variability. Any patients conditions with CAG repeats in the androgen receptor whose clinical diagnosis required revision at a later gene,13 single nucleotide polymorphisms in the stage were not included in the study. Controls with a HOXD gene,14 and an association between autistic family history of serious mental illness or other traits and/or autism spectrum conditions with single medical conditions such as type II diabetes, hyperten- nucleotide polymorphisms in sex-steroid related sion, cardiovascular or autoimmune diseases were genes.15 excluded. Other molecular factors in the etiology of autism spectrum conditions may not be sex-linked. Neuro- Psychological measures trophins such as brain-derived neurotrophic factor All participants were tested on the autism-spectrum (BDNF) are elevated in the blood of children with quotient (AQ),21 as a measure of the number of autistic autism, which may be associated with early brain 16 traits an individual possesses, the empathy quotient overgrowth and single nucleotide polymorphisms (EQ) and the systemizing quotient-revised (SQ-R)22 in in genes related to neural connectivity and neuro- 15 order to test the EMB theory at the cognitive level. trophic pathways may also be involved. In addition, Normally, 80% of people with autism spectrum several studies have identified an over-activation of 17 18 conditions score above a cutoff value of 32 (maximum mast and natural killer cells in autism spectrum = 50) on the AQ compared with only 2% for controls, conditions that may be associated with autoimmunity a finding that has been confirmed cross-culturally.23,24 or adverse immune interactions during critical peri- AQ predicts clinical diagnosis25 and has also been ods of brain development. Autism spectrum condi- shown to be elevated among parents of children with tions are also associated with familial autoimmune autism spectrum conditions,26 suggesting a heritabil- diseases and the presence of asthma, allergies and ity component. psoriasis during pregnancy.19 The interactions of these pathways in the nervous system are likely to be mediated by hormones and cytokines. Immunoassay profiling Here, we present the first systematic serum pro- We carried out HumanMAP profiling of 147 analytes teome profiling study of adults with the AS subtype of (see Supplementary Table S1) in serum samples from autism spectrum conditions. We had three major the AS and control subjects in a Clinical Laboratory objectives: (1) to test the EMB theory at the molecular Improved Amendments-certified laboratory at Rules level using a multiplex analyte profiling approach, (2) Based Medicine (Austin, TX, USA). This technology has already been applied successfully in several to test the prediction from the fetal androgen theory 27 that adult females with AS would have elevated clinical studies. Analytes were measured in multi- testosterone levels and (3) to determine whether plexes in 25–50 ml of serum samples. The assays were males and females with AS have distinct sex-specific calibrated using standard curves and raw intensity serum biomarker fingerprints. measurements converted to protein concentrations using proprietary software. Analyses were conducted under blind conditions with respect to sample Patients and methods identities and the samples were analyzed randomly Sample collection to avoid any sequential bias because of the presence Protocols for recruitment, collection of clinical sam- or absence of diagnosis, participant age, or age of ples and the test methods were carried out in material. compliance with the Standards for Reporting of Diagnostic Accuracy initiative.20 People with AS Statistics (n = 45) were recruited via the Cambridge Autism Analysis of variance was carried out on log-trans- Research Centre database of volunteers (www. formed data to investigate any interactions between autismresearchcentre.com), the National Autistic sex and diagnosis for each molecular analyte and Society (UK) and local autism social groups in the psychometric characteristic (AQ,
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