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Published online June 2, 2008
PEDIATRICS Vol. 121 No. 6 June 2008, pp. 1225-1229 (doi:10.1542/peds.2007-3000)
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SPECIAL ARTICLE

Autism and the Environment: Challenges and Opportunities for Research

Bruce M. Altevogt, PhDa, Sarah L. Hanson, BAa and Alan I. Leshner, PhDa,b

a Forum on Neuroscience and Nervous System Disorders, Institute of Medicine, Washington, DC
b American Association for the Advancement of Science, Washington, DC


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Autism spectrum disorder is a complex developmental disorder that dramatically affects the lives of patients and their families and the broader community. The causes of autism are unknown; however, evidence increasingly suggests that a complex interplay among environmental stressors, genetic mutations, and other biological factors likely plays a significant role in the development and/or progression of autism spectrum disorder. On April 18 and 19, 2007, the Institute of Medicine's Forum on Neuroscience and Nervous System Disorders hosted a workshop to provide a venue to bring together scientists; major sponsors of autism-related research; and members of the autism patient, family, and advocacy community to discuss the most promising and urgent scientific questions and opportunities. Broad participation by the autism community enriched the meeting significantly by contributing a valuable and personal perspective that is often missing from scientific meetings. It also began a much improved public–private partnership in which all stakeholders are represented. On the basis of the presentations and the discussions that followed, an array of important scientific opportunities were identified in 5 general categories: (1) opportunities to advance clinical research; (2) opportunities to enhance epidemiologic studies; (3) opportunities to improve the understanding of autism's pathology and etiology; (4) tools and infrastructure needs; and (5) opportunities for public–private partnerships. This workshop demonstrated that full public engagement can greatly enhance activities such as this workshop and its outcomes. Furthermore, we expect that this listing of scientific challenges, needs, and opportunities will help to frame a more comprehensive research agenda.


Key Words: autism • autism spectrum disorder • environmental biology • epidemiology • research agenda • public–private partnership

Abbreviations: ASD—autism spectrum disorder • IOM—Institute of Medicine • CDC—Centers for Disease Control and Prevention • IACC—Interagency Autism Coordinating Committee

Autism spectrum disorder (ASD) is a complex neurodevelopmental disorder that is usually diagnosed in children before age 3. Its hallmarks are impairments in social interaction; language skills, particularly in social communication; and imaginative play, along with a tendency toward various types of repetitive activities and fixated interests.1 The causes of autism are unknown; however, evidence now suggests that the environment may play a significant role in triggering autism, probably not on its own but through a complex interaction with genetic susceptibilities.

In response to a request from the US Secretary of Health and Human Services, the Institute of Medicine's (IOM's) Forum on Neuroscience and Nervous System Disorders (the forum) hosted a workshop on April 18 and 19, 2007, Autism and the Environment: Challenges and Opportunities for Research. The goal was to bring together scientists, members of the autism community, and the major sponsors of autism-related research to discuss the most promising scientific opportunities. Participants' presentations and discussions focused on improving the understanding of the ways in which the vast array of environmental factors, such as chemicals and infectious agents, may affect the development and progression of ASD. In addition, discussions addressed the infrastructure needs for pursuing the identified research opportunities, tools, technologies, and partnerships.

The workshop represented a partnership among members of the autism advocacy community, scientists, and policy makers. The engagement of the autism community provided a valuable and personal perspective that is often missing from scientific meetings. In fact, the autism community was involved in the early discussions that led to the secretary's request for this workshop. Throughout the workshop, in formal presentations and the discussion periods,* they contributed thoughtful and highly substantive comments and suggestions. Four of the 13 members of the workshop planning committee, which was responsible for organizing the workshop, identifying topics, and choosing speakers, were members of the autism community.{dagger} Moreover, autism community members were speakers and discussants, as well as workshop attendees. They reminded workshop participants about the urgency in addressing this serious health issue and actively participated in the scientific discussion.


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A recent survey by the Centers for Disease Control and Prevention (CDC) estimated that as many as 1 US child in every 150 may have an ASD, a group of diseases that includes autistic disorder and related disorders such as Asperger syndrome and pervasive developmental disorder-not otherwise specified.2 This number is dramatically higher than the prevalence estimates from studies conducted in the 1980s3 and early 1990s.4 Some have suggested that the increase does not reflect an increase in actual incidence of the disorder but rather is attributable to changes in reporting, clinical definitions, and services offered.5,6 Others believe that some or all of the increase indicates that the incidence rate, or rate of onset in children, is higher than 20 or 30 years ago.7 A number of workshop participants suggested that answering this question should be made a research priority.

It is not fully understood what causes autism or what may be leading to the reported increase in prevalence. In the past, much of the research into its causes focused on genetics, because evidence points to an undoubtedly large genetic component, but genes alone cannot account for its etiology.810 The majority of the evidence suggests that ASD represents a complex relationship between exposure to environmental stressors and genetic susceptibilities.

On the basis of the presentations and the discussions that followed, an array of scientific challenges, needs, and opportunities were identified in 5 general categories (Table 1). These opportunities are not a complete list; neither have they been adopted, endorsed, or verified as accurate by the National Academy of Sciences and thus should not be attributed to the National Academy of Sciences or the IOM. They do, however, represent a rich diversity of possible directions for future research and a model of how to bring together each of the key stakeholders to develop a common understanding of a problem and work together toward a common solution.


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TABLE 1 Scientific Opportunities and Needs Identified by Workshop Participants

 

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One of the major challenges identified by participants is the absence of diagnostic criteria that use quantifiable measures. Moreover, because ASD is not a unitary disorder but consists of many different syndromes, both research and proper clinical care require being able to organize patients with ASD into discrete categories on the basis of their phenotypes and response to treatments. Improved diagnostic tools would also increase the ability to look at trends over time or compare children from different environments.

The diversity of symptoms and symptom clusters attributed to autism emphasizes that there is not just 1 type of autism but rather a collection of different variants, each with its own set of characteristics and, presumably, etiologies. The inability to identify and stratify biologically meaningful subpopulations has limited research into the causes of autism. Thus, several workshop participants highlighted the need to develop autism phenotypes that may be used to identify clinically meaningful subtypes, looking at onset, clinical presentations, the associated symptoms, and the clinical course. Participants identified several potential strategies that could be used to investigate potential subtypes, including but not limited to analysis of genetic data, analysis of biological samples (eg, blood, urine), metabolic profiling, and stratification and analysis on the basis of comorbidities.

A related theme that speakers emphasized was the need to identify effective biomarkers for different aspects of autism. These biomarkers could then be used in a variety of ways, including improving ASD diagnosis, identifying particular phenotypes and subphenotypes, helping to determine the pathophysiologic mechanisms that underlie specific phenotypes, predicting and tracking the effectiveness of various treatments, and aiding in the identification and development of novel therapeutic interventions.

A variety of treatment approaches were described during the workshop. In addition to the need to study their effectiveness in more detail, studying how different patients respond to various treatment protocols may provide a tool to gather insights into the causes of autism. Workshop participants also discussed analyzing older populations of individuals with ASD and the opportunities that such an analysis would likely offer in terms of the progression of ASD, subpopulation data, and baseline data on the characteristics of ASD in its fully manifested state.


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Epidemiologic studies offer 1 major strategy to identify the genetic and environmental underpinnings of autism, but the complexity of autism makes those kinds of studies extremely difficult to design and carry out. Although several epidemiologic studies are under way, many were not specifically designed to investigate potential gene–environment interactions that may contribute to autism; therefore, participants suggested that a review and assessment of ongoing and completed epidemiologic studies would be of great value. There is a need to help identify what the complementary and overlapping goals are for each study, where the gaps are, and the potential of studies that have not yet been funded or solicited in helping to address these issues. Participants also highlighted a need to improve the infrastructure and tools available to promote pooling and sharing of data. Along these efforts, the importance of improving and standardizing criteria that could be used to define and screen cohorts was stressed.

Several speakers also pointed out the importance of performing epidemiologic studies of specific subpopulations that display special characteristics (eg, high-risk individuals, discordant twins, high-risk siblings). Study populations might include, for example, children who were exposed prenatally to infectious diseases or toxicants from environmental exposures in an effort to identify etiologic factors; or if autism prevalence is found to be higher in certain groups of people, then a specific epidemiologic study of that cohort could provide insight into uncovering a cause that otherwise may be missed. Large, long-term longitudinal studies such as the National Children's Study, which will examine the impact of environmental factors on the health and development of >100000 children, also offer great potential to provide important data and insights.11,12

The opportunities provided by cohorts established through natural experiments were also emphasized in the workshop. Natural experiments are established in a variety of ways. Examples include examining historical events that result in people's being exposed to harmful or protective factors; examining specific populations that may offer unique characteristics, such as the Amish; or comparing distinct populations, such as Hispanic versus non-Hispanic individuals. Furthermore, additional analysis of cohorts from foreign countries, both industrial and developing, also offers many opportunities. The importance of well-defined standardized cohorts is exemplified in these cases.

As previously mentioned, the absence of authoritative data about the incidence of ASD continues to be a major obstacle and burden for the field. Individuals from each stakeholder sector represented—policy makers, basic researchers, epidemiologists, and patient advocates—highlighted the need to obtain improved time trends data to begin to answer this important question. This includes improved and expanded longitudinal studies as well as sophisticated retrospective meta-analysis on existing prevalence data.


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In discussing potential mechanisms for how genes and environment could combine to cause autism, some speakers focused particularly on the possible role of infections. Another focus was on environmental toxicants that might affect cellular mechanisms in a way that alters brain development in the fetus. For example, the redox state—the balance between reducing agents and oxidizing agents in a cell—in developing neuronal cells may play a role in the cause of autism. In addition, several speakers highlighted the immune system and how immunologic susceptibilities may play a role in the development of autism. One specific example that was cited as a largely unexplored opportunity is the use of new technologies, including genome sequencing and phylogenetic analysis, to identify potential novel microbial stressors that may be affecting the development or progression of ASD.


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Several speakers highlighted the importance of the proper collection and storage of biological samples. A few efforts are currently under way, including the National Institute of Mental Health's Human Genetics Initiative, which has an extensive repository of DNA and cell lines from people with autism.13 As of January 2008, it will have >1600 samples available. These samples could be used to probe models of potential gene–environment interactions; however, even with these current resources, it was suggested that expanded tissue and biological sample repositories are needed. Additional protocols would enable the collection of information on both potential genetic predisposition and environmental exposure, with an emphasis on collecting appropriate control samples. It is also important that the sample collection be forward-looking. The collection of biological samples relates to a theme that was discussed throughout the meeting, which is the need to establish more large-scale efforts across domains. For example, standardized sample collection could be better integrated into ongoing epidemiology studies.

The value of developing and expanding registries of children and adults with ASD was underscored by many speakers and workshop participants. These registries could be used in a number of ways, from generating hypotheses to identifying potential patients. The need to expand the availability of eligible individuals for clinical trials could be helped by increased participation in registries, for example. Although not many potential treatments will be ready to examine soon, the importance of having the resources available when a potential treatment is ready for a large-scale clinical trial cannot be underemphasized. Recognizing this need, in January 2006, Autism Speaks partnered with the Kennedy Krieger Institute to establish the Interactive Autism Network, which was envisioned to provide the necessary coordinating role and infrastructure to support research partnerships between patients and the research community.

To determine which environmental exposures may be involved in autism, speakers discussed various tools and technologies that are available for monitoring and evaluating environmental exposures, including some cutting-edge technologies that have recently become available. Exposure can be assessed in a variety of ways: chemicals that appear over time can be monitored through environmental sensors in a place of interest; personal sensors, such as dosimeters, can track of an individual's exposures; and molecular-level sensors can detect thousands of substances down to the level of individual molecules. In addition, more "traditional" technologies were discussed, including high-performance liquid chromatography, mass spectroscopy, 2-dimensional gas chromatography, and microfluidics.

Because relevant technologies are rapidly increasing in power and sensitivity to the point that it is becoming easy to test for thousands of substances at 1 time, some suggested that searching for everything, instead of focusing on just a subset of substances that seem likely to be involved, is the best option. To do this, speakers suggested adapting biosensor technologies. Finally, as mentioned previously, some believe that given how rapidly the technology is improving, it may be better to spend the limited resources on beginning to establish comprehensive biorepositories so that samples will be ready once improved assessment tools become available.

No matter which of these options is best, 1 of the most pressing needs for the autism field is to attract both environmental biologists and individuals with expertise in bioinformatics. In the past, autism was able to attract the best and brightest geneticists by providing funding incentives and convincing them that there were worthwhile problems to address in the autism area. Although it will be important to establish a pipeline that draws and develops young researchers in the area of autism and environmental exposures, that will take a number of years. The best short-term strategy is to attract researchers from other fields, as was done with genetics.

To transform autism research into a truly interdisciplinary field, several participants said that incentives are needed to attract top researchers from diverse domains, including epidemiology, toxicology, developmental biology, and environmental science. Funding that promotes an interdisciplinary approach will be important. Several participants made the concrete suggestion that continued support must be ensured for strong centers of excellence in children's environmental health.


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The effective involvement by the autism advocacy community contributed an extremely valuable perspective that is often missing from scientific meetings and demonstrated the beginning of a true public–private partnership. Throughout the workshop, in formal presentations and discussion periods, members of the autism advocacy community offered thoughtful and substantive comments and suggestions; the substantive suggestions discussed in this article reflect their input virtually as much as that of the scientists who were present. Not only did they keep the children, who are the victims of the disease, in the forefront of the discussions, but also they made it clear that the organized autism network of patients, parents, and providers wants to help both the scientific community and policy makers to develop and prioritize a more effective and relevant research agenda. Among other insights, they reminded the group of the significant portion of research funding that the autism community has contributed and are making available to researchers.

Additional steps will be needed to ensure that the scientific, policy, and advocacy communities become more active partners in framing the questions that will drive the research agenda into the future. Although this can occur successfully through many models, an example highlighted during the workshop is the Defense Department's Breast Cancer Research Program. In response to a 1997 IOM report,14 this program developed a peer-review system that included cancer survivors in the examination of its programmatic goals that includes cancer survivors in the review panels.15 This step helped to incorporate the needs of affected individuals into policy and research agenda development. One venue for continuing involvement of stakeholders in the autism research agenda is the Interagency Autism Coordinating Committee (IACC). Established by the Children's Health Act of 200016 and reestablished by the Combating Autism Act of 2006,17 the IACC includes stakeholder representatives, and the advocacy community has a history of strong involvement in IACC activities. The Combating Autism Act increased the number of patient/parent representatives and will be an important avenue for ongoing collaborations.

Emphasis was also placed on the importance of improved coordination of efforts undertaken by all stakeholders. Workshop participants stressed the importance for public and private funding agencies—government agencies and autism organizations, such as the National Institutes of Health, CDC, Autism Speaks, and the Simons Foundation—to coordinate their efforts. Private-sector contributions to research are substantial; at least 20% of basic research funding for autism is supported by the private sector. There are many noteworthy organizations within the autism community, and it is important that the efforts and perspectives of these community members be integrated into a common set of goals.

This workshop was an important milestone in the development of a research agenda to examine the potential impact of the environment in the development and progression of autism, but it is only a beginning. As various actors move forward in developing and implementing the research agenda, we urge that all stakeholders be included in all critical discussions. Although many scientific opportunities and aspects of autism and its cause were discussed, we consider the IOM workshop to have been a significant testimony to the concept of full public engagement and recommend it as a model to others.


    ACKNOWLEDGMENTS
 
This workshop was funded by the membership of the IOM Forum on Neuroscience and Nervous System Disorders with supplemental support from the National Institutes of Health (National Institute of Child Health and Human Development, National Institute of Environmental Health Sciences, National Institute of Mental Health, and National Institute of Neurological Disorders and Stroke) and the CDC (grant N01-OD-4-2139, Task Order 175).

We are extremely grateful for the efforts and dedication of the workshop planning committee and everyone who participated in the workshop, especially the speakers.


    FOOTNOTES
 
Accepted Oct 10, 2007.

Address correspondence to Bruce M. Altevogt, PhD, Institute of Medicine, Forum on Neuroscience and Nervous System Disorders, 500 Fifth St, NW, Washington, DC 20001. E-mail: baltevogt{at}nas.edu

The authors have indicated they have no financial relationships relevant to this article to disclose.

The responsibility for the content of this article rests with the authors and does not necessarily represent the views of the Institute of Medicine and its committees and convening activities.

* The workshop agenda and presentations may be viewed at www.iom.edu/?id=42481. Back

{dagger} Planning Committee membership: Alan Leshner, Chair (American Association for the Advancement of Science), Duane Alexander (National Institute of Child Health and Human Development), Mark Blaxill (SafeMinds), Laura Bono (National Autism Association), Sophia Colamarino (Autism Speaks), Eric Fombonne (McGill University), Steven Hyman (Harvard University), Judy Illes (University of British Columbia), Thomas Insel (National Institute of Mental Health), David Schwartz (National Institute of Environmental Health Sciences), Susan Swedo (National Institute of Mental Health), Alison Tepper Singer (Autism Speaks), and Christian Zimmerman (Boise State University and Neuroscience Associates). Back


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  17. Combating Autism Act of 2006. §843. 109th cong, 2nd sess; 2006

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