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Applying Hill's Criteria to the Study of Autism Spectrum Disorders and Exposure to Mercury Abstract Applying Hill’s criteria to the Study of Autism Spectrum Disorders and exposure to mercury This work was supported by the Canadian Institutes of Health Research (Meetings, Planning, and Dissemination Volume 18, Number 1, 2012 Grant, grant number 90876; H. Ouellette-Kuntz, principal applicant). Authors Abstract Virginie Cobigo, Purpose. Autism Spectrum Disorders (ASDs) are neuropsych­ Malia Su-Qin Murphy, iatric disorders that include Autistic Disorder, Asperger syn­ Iwona A. Bielska, drome and Pervasive Developmental Disorders – not otherwise Hélène Ouellette-Kuntz specified (PDD­NOS). Prevalence rates of ASDs are reported to have increased in the last decade, raising concern amongst Department of Community researchers, service providers, policymakers, and families. While Health and Epidemiology, current aetiological research is exploring the interface between Queen’s University, genetic and environmental factors, exposure to heavy metals, in Kingston, ON particular mercury has retained public interest. methods. A systematic review of publications from 1980 to 2010 inclusive was used to examine the hypothesized link between ASD and mercury exposure. Hill’s criteria for causa­ tion were applied to critically appraise the reviewed studies. Results. Reviewed studies failed to demonstrate strength and consistency of association as well as establish a temporal link between the onset of ASD symptoms and mercury exposure. conclusions. The risk of developing and being diagnosed with an ASD as a result of mercury exposure remains unclear Correspondence because of methodological flaws in studies conducted to date. Rigorous research is needed to provide adequate information [email protected] to families, clinicians and decision­makers. They must be pro­ vided with up­to­date, critically appraised information to help them make informed decisions. Keywords Autism Spectrum Disorders (ASDs) are neuropsychiatric autism spectrum disorders, disorders that include Autistic Disorder, Asperger syndrome heavy metals, and Pervasive Developmental Disorders – Not Otherwise mercury, Specified (PDD-NOS) (DSM-IV-TR) (American Psychiatric aetiology, Association (APA), 2000). Reported prevalence rates of ASD Hill’s Criteria are inconsistent across the literature and may range from 10.1/10,000 to 64.9/10,000 (Bryson, Clark, & Smith, 1988; Fombonne, Zakarian, Bennett, Meng, & McLean-Heywood, 2006; Ouellette-Kuntz et al., 2006). Prevalence rates are reported to have increased in the last decade raising con- cern amongst researchers, service providers, policymakers, and family members (Ouellette-Kuntz et al., 2007; Rice et al., © Ontario Association on Developmental Disabilities Autism and Mercury Exposure 21 2007). A review of 43 epidemiological studies a lack of evidence to prove these three criteria revealed that only a small fraction (0% to 16.7%; is not sufficient to rule out the causal relation- mean = 5.9%) of the cases of Autistic Disorder ship. Experimental studies (criterion 8) provide could be related to any known aetiologic- greater evidence of a causal link but may be ally significant medical condition (Fombonne, unethical to perform in neuropsychiatry since 2005). While current aetiological research is it is unconceivable to induce some form of brain exploring the interface between genetic and dysfunctions experimentally in humans. environmental factors, exposure to heavy met- als, in particular mercury, has retained public interest (Hertz-Picciotto et al., 2006). This paper criteria for causation Between aims to improve critical thinking towards stud- mercury and ASD ies investigating the causal link between ASD and exposure to mercury by applying the nine Mercury is just one of a handful of heavy met- criteria for causality as defined by Hill to the als that have been suggested as environmental literature related to these associations (Hill, contributors to the development of ASD. The 1965). Hill’s criteria include: (1) the strength heightened public interest regarding the until- of the association, (2) the consistency of the recent presence of thimerosal (a mercury-based observed association, (3) the specificity of the preservative) in widely distributed vaccina- association, (4) the temporal relationship of the tions amongst other sources of exposure raises association, (5) a biological gradient or dose- concern over the insufficient evidence tying response curve, (6) the biological plausibility, the heavy metal to the manifestation of ASD. (7) the coherence with the current knowledge, In this next section, a brief comment is made (8) experimental or semi-experimental evi- on issues relevant to each of Hill’s nine crite- dence, (9) and the analogy with similar evi- ria regarding the association between ASD and dence. The strength and the consistency of the mercury. association are two criteria that must invariably be considered to prove causation (Hill, 1965). Other criteria might be difficult to establish or criterion 1: Strength irrelevant to the nature of the observed associa- of the Association tion, but should nevertheless be systematically examined. If evidence exists for the remaining The strength of an association is the statisti- seven criteria, conclusions may be drawn with- cal or clinical significance of the association, is out hesitation, although the lack of evidence observed in a well-defined population but does does not nullify a causal association. not occur to the same extent in an appropriate control group. Case-definition, sample size and In neuropsychiatry, four of Hill’s nine criteria statistical power are thus crucial to determine are considered critical to assess causality: the the strength of an association. Differences in strength of the association (criterion 1), the participant selection and identification pro- consistency of the observed association (crite- cedures across studies are key methodologi- rion 2), the biologic rationale (criterion 6), and cal issues that must be considered. ASD was the temporal relationship of the association (cri- first introduced in the third edition of the terion 4) (van Reekum, Streiner, & Conn, 2001). Diagnostic and Statistical Manual (DSM-III) in Arguments of a biologic gradient (i.e., severity 1980 (American Psychiatric Association (APA), of symptoms increases with exposure; criteri- 1980) and subtypes and diagnostic criteria have on 5) and specificity of the relation between the been revised several times since (DSM-III-R; causal agent and the outcome (criterion 3) may DSM-IV; DSM-IV-TR) (APA,1987; APA, 1994; not be feasible to prove, since symptom severity APA, 2000). Two- to threefold variation in the is difficult to determine and multiple causal fac- prevalence rates of ASD can result from apply- tors are generally identified for one neuropsy- ing different diagnostic criteria to the same chiatric disorder. Coherence with known facts survey data (Kielinen, Linna, & Moilanen, (criterion 7) and analogy with similar evidence 2000). Social and demographic characteris- (criterion 9) might add to our understanding of tics of the cases with ASD may also influence the association; however, aetiological under- study results. Attention should be given to the standing in neuropsychiatry is still limited and participants’ gender as the male: female ratio v.18 n.1 cobigo et al. 22 is approximately 4:1, with a more pronounced from all possible sources, but not all of them difference among individuals with intellectual can provide information on past exposures disabilities (Fombonne, 2005). To appraise the (World Health Organization (WHO), 2006). multiple factors that could impact the strength Mercury accumulates in the bones and teeth, of the observed association, a systematic review and can be excreted through sweat, nails, urine of the literature on ASD and exposure to mer- and feces. Measurement of heavy metals from cury was conducted. Systematic reviews are body tissues is not only affected by tissue- designed to assess the strength of the observed specific half-lives, but also may largely be a associations as they help in collecting and cri- result of differential accumulation and excre- tiquing relevant methodological information in tion capabilities and mechanisms amongst dif- all selected studies. ferent populations (Axel Weiner & Nylander, 1993; Grandjean, PAL, & White, 1995; Holmes, criterion 2: consistency of the Blaxill, & Haley, 2003; Kern, Geier, Adams, & observed Association Geier, 2010). The reported half-lives of mercu- ric compounds in blood and body tissues are variable. Data from five publications found the An assessment of consistency requires deter- half-life of methyl mercury in blood or hair mining whether the association has been to range from 45 to 70 days (Al-Shahristani & repeatedly observed by different persons, in Shihab, 1974; Kershaw, Dhahir, & Clarkson, different places, circumstances and times (Hill, 1980; Miettinen, Rahola, Hattula, Rissanen, 1965). Methodological issues may explain dis- & Tillander, 1971; Sherlock, Lindsay, Hislop, crepancies, but if no reason justifies discrepan- Evans, & Collier, 1982; Smith et al., 1994). cies, evidence seriously undermines the argu- Therefore, prenatal and early childhood expo- ment of causation (van Reekum et al., 2001). sures are not likely to be identified through Systematic reviews are particularly useful in blood or hair mercury levels measured later in assessing consistency across studies while tak- life. Mercury levels in bones and teeth provide ing into account methodological issues. more information
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