Autism spectrum disorder (ASD) is a complex, behaviorally heterogeneous
neurodevelopmental disorder that can impact nearly every area of functioning. Individuals with ASD are reported to experience difficulties adapting to and feeling at ease in their environment, as well as navigating between preferred patterns of behavior and societal expectations of proper conduct (Jones & Meldal, 2001; Trembath, Germano, Johanson, & Dissanayake, 2012). An official diagnosis of ASD is characterized by core symptoms including (a) persistent deficits in social communication and social interaction across multiple contexts and (b) restricted, repetitive patterns of behavior, interests, or activities, which may include hypo- or hyper-reactivity [i.e., hyperresponsiveness] to sensory information from the environment (American Psychiatric Association, 2013). Common co-morbid symptoms include elevated levels of anxiety (van Steensel & Heeman, 2017), impaired life skills (Bal, Kim, Cheong, & Lord, 2015), and compromised mental health (Tick et al., 2016). When combined, both core and co-morbid features can be extremely detrimental to individuals’ quality of life and ability to form meaningful connections to those around them.
The coexistence of three features: sensory hyperresponsiveness, restricted, repetitive patterns of behaviors, interests, or activities (denoted hereafter as RRBs), and anxiety may have a particularly deleterious effect. Their presence often corresponds with situations that are
to focus, and precipitating the need to ‘escape’ in order to cope (Halim, Richdale, & Uljarević, 2018). These three features are closely related both empirically and theoretically. Sensory hyperresponsiveness and RRBs share the same diagnostic classification and are both central to hypotheses of arousal regulation (Turner, 1999). Signs of aversion to or escape from certain situations may be attributed to either hyperresponsiveness (Baranek, Boyd, Poe, David, & Watson, 2007) or anxiety (Davis III et al., 2010), while reduced participation in the surrounding environment may be a sign of anxiety (Wood & Gadow, 2010) or RRBs (Patriquin, MacKenzie, & Versnel, 2019). In addition, shared neurological mechanisms may underlie the expression of two or more of these constructs (Boyd et al., 2010).
Various approaches provide different layers of insight into each of these features. Animal modelling allows for more controlled genetic manipulation and direct examination of subsequent phenotypic expression that mimics features of ASD (Crawley, 2012). Neurological studies investigate certain localized brain regions or alterations in neural connectivity (Muhle, Reed, Stratigos, & Veenstra-VanderWeele, 2018). Methods such as questionnaires or direct
observation help characterize these features behaviorally, while self-reported experience via semi-structured interviews or focus groups (DePape & Lindsay, 2016) detail how the features manifest in everyday lived experience.
Sensory Hyperresponsiveness
In general, the literature characterizes sensory hyperresponsiveness as an increased sensitivity to stimuli in the environment. Studies that rely on mice or rat models measure sensory perception thresholds by determining the amount of stimulation required for a tail flick or paw retraction (Favre, Markram, & Markram, 2019). Studies with human subjects similarly measure thresholds of sensory perception via the magnitude of startle response to sensory stimulation
Neurophysiological techniques are used to calculate the amplitude of brain wave responses to stimuli, which are often heightened in individuals with ASD who exhibit hyperresponsiveness compared to the typically developing population (Takarae., Sablich, White, & Sweeney, 2016). Standardized behavioral assessment through observation (e.g., Sensory Processing Assessment; Baranek, 1999) or questionnaires (e.g., Sensory Profile; Dunn, 1999) describes signs of sensory hyperresponsiveness, such as avoiding certain situations or exhibiting defensive reactions, such as covering ears to certain sounds (Baranek et al. 2007; Watling, Deitz, & White, 2001). Avoidant and defensive behaviors are also corroborated by many self-reports of the hyperresponsive experience (Robertson & Simmons, 2015).
Restricted Interests and Repetitive Behaviors
RRBs are commonly classified as either lower-order repetitive motor behaviors (Gal, Dyck, & Passmore, 2010) or higher-order behaviors such as an insistence on sameness, strict adherence to routines and rituals, and circumscribed interests (Kerns et al., 2014; Lane, Molloy, & Bishop, 2014). These are often captured via observation or questionnaire measures such as the Repetitive Behavior Questionnaire-2 (Leekam et al., 2007) or the Repetitive Behavior Scale- Revised (Bodfish, Symons, & Lewis, 1999; Lam & Aman, 2007). Neurological evidence reveals a multitude of brain regions and altered patterns of connectivity that are implicated in the
expression of RRBs (for review studies, see Amaral, Schumann, & Nordahl, 2008 and Traynor & Hall, 2015). Additionally, self-reported accounts describe repetitive behaviors as an important outlet for self-regulation, and the need for order and routine to support functioning in daily life (Cesaroni & Garber, 1991). Studies using mice or rat models approximate RRBs through behaviors such as repetitive locomotor activity or excessive self-grooming (Bechard & Lewis, 2012).
Anxiety
Anxiety in individuals with ASD has been characterized in a number of ways. Many studies address anxiety by its own clinical diagnoses (e.g., separation anxiety, social anxiety, specific phobia; Gillott, Furniss, & Walter, 2001). Other studies describe common behavioral traits affiliated with anxiety such as pacing or withdrawal (Kerns & Kendall, 2012). It has also been proposed that individuals with ASD may display more somatic symptoms of anxiety than those in the non-ASD population, experiencing more frequent panic attacks, headaches, or stomachaches, for example (Kerns & Kendall, 2012). Common behavioral measures of anxiety in ASD include the Spence Children’s Anxiety Scale (Spence, 1997; Gillott, Furniss, & Walter, 2001) and the Child Behavior Checklist (Achenbach & Rescorla, 2001; Read et al., 2015). Animal models approximate anxiety through signs of fear-related behavior, including reduced exploration or reduced marble burying activity (Markram, Rinaldi, La Mendola, Sandi, & Markram, 2008). Notably, individuals with ASD highlight anxiety as one of the most difficult aspects of their condition, as it often impairs their ability to remain calm and focused, creates distortions in thinking, and leads to negative perceptions of themselves and their experiences (Trembath et al., 2012).
Study Aim
Collectively, the presence of these three COIs in individuals with ASD can be extremely detrimental to positive outcomes. Therefore, it is vital to understand the qualities that unite these features and influence their expression. However, there has not yet been a review in the literature to systematically evaluate how the associations among them are currently characterized across different disciplines, which is necessary to fully capture the complexity of these phenomena and strengthen the evidence base that may exist. This study asked the following research question:
What factors contribute to the combined expression of sensory hyperresponsiveness, restricted interests and repetitive behaviors, and anxiety in ASD?
This review is considered ‘integrated’ both in terms of including a wide variety of methodological approaches for review (Broome, 1993) and in terms of pursuing an analytical strategy that prioritized thematic similarity over methodological category (Sandelowski, Voils, & Barroso, 2006). Combining both quantitative- and qualitative-oriented studies in systematic reviews is becoming increasingly popular in applied fields, as it bridges the gap between the strong evidence derived from highly-controlled laboratory studies and its relevancy to individuals in more naturalistic contexts (Harden & Thomas, 2005). Expanding the
methodological scope in systematic reviews also coincides with a burgeoning of possibilities in the types of research questions that can be answered (Harden, 2010; Pearson et al., 2015). 2.2 Method
This study used an integrative systematic review process to gather and analyze sources of literature that concurrently showcased associations among hyperresponsiveness, RRBs, and anxiety. The review aimed to be inclusive of a broad array of methodologies in order to evaluate consistent themes that emerged across disciplines. The procedure for an integrative systematic review maintains many of the features of a traditional systematic review methodology
(Siddaway, Wood, & Hedges, 2018). This study followed the seven stages as outlined by Harden and Thomas (2010): 1) formulate a review question: 2) establish inclusion and exclusion criteria; 3) develop a review protocol; 4) conduct a literature search using various databases; 5) describe key features of included studies; 6) address the quality of included studies; and 7) synthesize findings.
Literature Search
Articles were searched from six databases that spanned multiple scientific disciplines. Databases included PsycINFO, PubMed, ERIC, CINAHL, SCOPUS, and the Social Science and Humanities Indices of Web of Science. The search terms used are listed in Table 2.1. For
PubMed, MeSH search terms were used (Lu, Kim, & Wilbur, 2009). Inclusion required the presence of at least one of the terms from each of the four categories (diagnostic, sensory, RRBs, and anxiety) in either the title or the abstract to be considered for review. No restrictions were put on the search regarding year published, in order to avoid potentially excluding articles that could provide important historical context. Reference lists from articles that met inclusion for the final analysis were manually searched for any titles that were potentially missed by the database search. As these two methods did not yield a large number of qualitative articles, relevant journals from 2000-present were also hand-searched by the first author.
Articles were uploaded into Covidence software, which allows for an initial screening round based on titles and abstracts to eliminate non-relevant articles followed by a full screening round using the full text. Both rounds were completed independently by two qualified reviewers (myself and a research assistant) with multiple years of research and clinical experience working with individuals with ASD. The full search and screening procedures are detailed in Figure 2.1. A total of 22 articles were ultimately accepted in the final analysis, using the full list of inclusion and exclusion criteria provided below:
Inclusion criteria:
1. Primary condition investigated in the article is ASD or some variant thereof (PDD- NOS, autistic disorder, Asperger's disorder).
b. Animal models will have comparable phenotypic expression for the purpose of informing factors specifically implicated in ASD.
2. All three constructs of interest are featured within the article.
a. Articles using deductive reasoning (i.e., quantitative methods) will include measurement and analysis of all three COIs.
b. Articles using inductive reasoning (i.e., qualitative methods) will include all three COIs in results and discussion.
c. Mixed methods articles will follow the above criteria for each respective method.
3. Articles must be in English or have an available English version.
4. Articles must be peer-reviewed, original research or a dissertation study. Exclusion criteria:
1. Review articles
2. One or more constructs of interest (COIs) are not featured in the article (i.e., only one COI, or a combination of only two out of the three COIs were featured based on the criteria above).
3. COIs are not featured more prominently than other characteristics of ASD (i.e. the focus of the study spans a multitude of areas including those not relevant to this review, such as social interaction, maladaptive behavior, etc.).
Two trained reviewers independently rated the methodological quality of each article using the Mixed Methods Appraisal Tool (MMAT; Hong et al., 2018; Pluye, Gagnon, Griffiths, & Johnson-Lafleur, 2009). This tool allows for each study type (classified in the MMAT as qualitative, non-randomized, quantitative descriptive, mixed methods, and randomized controlled
trials) to be evaluated according to their appropriate validity and reliability criteria. Non-
randomized intervention studies, cohort studies, case-control studies, and cross-sectional analytic studies are included in the quantitative non-randomized category. Examples of quantitative descriptive studies are incidence or prevalence studies without a comparison group, survey studies, case series, or case reports (Hong et al., 2018). However, the authors note that qualities of some cross-sectional designs may overlap with criteria from both the non-randomized and quantitative descriptive categories.
Approach to Analysis
There are a few established approaches to collating and evaluating articles included in a systematic review that incorporates multiple methods (for an overview, see Pearson et al., 2015). This review uses an integrated design, which synthesizes studies based on similar themes in order to prioritize addressing the overall research question above the methods used
(Sandelowski, Voils, & Barroso, 2006). In accordance with this approach, data was assimilated throughout the entire analytical process (as opposed to being separated and synthesized
according to quantitative or qualitative methods). Qualitizing techniques (i.e., translating results from quantitative data into descriptive form) were used to create a complete set of data in the same narrative format (Onweugbuzie & Teddlie, 2003; Tashakkori & Teddlie, 1998). The results were then reviewed multiple times and categorical codes were created based on patterns that emerged. Codes were then sorted into over-arching themes that best characterized the associations among the three constructs of interest (Harden & Thomas, 2005).
2.3 Results
Quality Appraisal
randomized (n=10; two of which were intervention studies), and mixed methods (n=1). None of the studies used a randomized controlled trial design. Scores on the MMAT were averaged across reviewers on a scale of 1 to 5, with 5 being the highest attainable score. Percent agreement was calculated for qualitative studies (93.3%) and quantitative studies (73.3%). All studies met at least four of the five quality criteria for their respective methodology, with seven studies
receiving a score of 5, eight studies receiving a score of 4.5, and seven studies receiving a score of 4. No studies received an average score lower than 4 points. Of the articles that did not receive the highest score, limitations included lack of clarity on the type and validity of the
methodological approach, caregiver-informed ASD diagnosis, over-interpretation of results based on the sample size, and absence of full demographic information.
Structural Relationships among the Constructs of Interest
Three distinct patterns depicted the structural relationships among the three constructs. Differences stemmed from the purpose of each study, the method that was chosen (e.g., separate assessments for each construct versus constructs embedded within descriptive narratives), and the format of the results. The main structures identified were parallel, relational, and contingent. A parallel structure treated all three constructs of interest separately within the study, generally measuring changes in each across time or before and after an intervention. More often, a relational structure was used to compare the constructs to each other in some way. Lastly, a contingent structure described the constructs in such a way that their expressions were dependent upon each other or some other variable. This category is further divided into three sub-groups: relative (i.e., expression of one was greater or less relative to the other or some other factor), threshold dependent (i.e., expression depended on others reaching a critical threshold), and mediated (i.e., expression of one fully or partially explained associations between the others). A
summary of the results of each article according to their structural category is reported in Table 2.3.
Overall Themes
Three overall themes best characterized the factors that influenced the combined
expression of sensory hyperresponsiveness, RRBs, and anxiety across studies. These were: COI function is interwoven with the broader social context, COIs are heavily contingent on the predictability of environmental factors, and COIs overlap with cognitive and behavioral coping strategies.
COI function is interwoven with the broader social context. Although articles with content explicitly focused on social aspects of ASD were excluded from analysis, the broader social context nevertheless exhibited a strong presence among the studies in this review. The three constructs of interest were not only intra-connected, but their expressions were also a function of the social system of which the individuals with ASD were a part. Dedicating the intense focus and concentration that is needed in social situations reduced the ability to filter out sensory distractions such as background noise, amplifying their degree of intrusion (Ladon, Shepherd, & Lodhi, 2016). The higher demand on information processing via the sensory system required in social encounters often ramped up anxiety that could be reduced through performing repetitive sensory-motor behaviors (Ozsivadjian, Knott, & Magiati, 2012; Shirley, 2018).
Mice with an ASD-like phenotype exhibited decreased social interaction and increased self-directed grooming activities that parallel RRBs in ASD (Wurzman et al., 2015). In a separate study, lower anxiety in a rat model of ASD corresponded with less fixation on the physical environment and a greater preference for social exploration (Schneider, Turczak, & Przewłocki, 2006). Comparable reports from individuals with ASD suggested that engaging in
modalities, decrease anxiety, and support individuals in their ability to concentrate on social aspects of their environment (Ozsivadjian, Knott, & Magiati, 2012; Shirley, 2018; Smith & Sharp, 2013).
Some individuals also reported performing repetitive motor behaviors in private to avoid experiencing the social stigma attached to them, or not performing them at all out of fear of judgment, increasing anxiety and preventing an important coping mechanism for sensory overstimulation (Ozsivadjian, Knott, & Magiati, 2012). A study investigating specific subtypes of anxiety reported greater socio-communicative anxiety in young adults with ASD compared to those with anxiety but not ASD (Halim, Richdale, & Uljarević, 2018). Conversely, anxiety was reduced when individuals with ASD felt understood by their peers and vice versa. In an
intervention to address adverse sensory experiences, participants responded positively to an increased awareness of how their sensory experiences may differ from those around them. Participants also reported that learning the skills needed to explain this difference to others greatly contributed to their sense of coping efficacy (Edgington, Hill, & Pellicano, 2016). However, it is noteworthy that a study by Black and colleagues (2017) found no evidence for hyperresponsiveness mediating the association between social anxiety and insistence on sameness.
COIs are heavily contingent on the predictability of environmental factors. Both reports by individuals with ASD and studies using animal models similarly concluded that the unpredictability of novel situations could be anxiety-inducing due to the amount of new stimuli that needed to be processed (e.g., Landon, Shepherd, & Lodhia, 2016), or due to difficulty filtering out relevant stimuli (and therefore processing a greater sensory load; Favre et al., 2015; Schneider, Turczak, & Przewłocki, 2006; Wurzman et al., 2015). Furthermore, some studies
reported a circular effect wherein elevated anxiety combined with increased sensory sensitivity caused certain stimuli to be experienced with even greater intensity, perpetuating discomfort and ramping up anxiety even more in unpredictable environments (Jones, Quigney, & Huws, 2003; Smith & Sharp, 2013). A study by Chamberlain and colleagues (2013) reported a higher level of baseline sensitivity in individuals with ASD and further concluded that, beyond predictability, certain contexts may be experienced as ambiguous because atypical sensory processing disrupts the ability to interpret cause-and-effect between an action on the environment and the sensory feedback received, thus leading to heightened anxiety and increased performance of RRBs. Conversely, animal modelling suggested that prolonged interaction with the environment
resulted in reduced RRBs, decreased anxiety, and a better-adjusted sensory system to painful and non-painful stimuli (Schneider, Turczak, & Przewłocki, 2006).
When anxiety was not present, often in environments that were predictable, sensory experiences and RRBs were engaged in positively, often eliciting fascination and pleasure (Smith & Sharp, 2013). A study by Joosten, Bundy, and Einfeld (2012) investigated behavior in various classroom environments. The researchers concluded that children with ASD exhibited less anxiety and performed repetitive motor behaviors as a result of increased sensory
engagement when given the liberty to direct their own play during free time. Conversely, in times of classroom transition, anxiety became heightened and replaced sensory engagement as the main impetus for engaging in repetitive motor behaviors. Although the researchers did not draw specific conclusions about why the different motivators for engaging in RRBs were observed in different classroom contexts, other studies in this review (e.g., Jones, Quigney, & Huws, 2003; Smith & Sharp, 2013) discussed the inherent satisfaction that individuals with ASD may achieve when engaging in preferred repetitive motor behaviors, which are opportunely
provided during the context of free play. During transitional periods, the immediate environment became much more chaotic and experiences became less predictable and controllable, at which point RRBs addressed a need to manage anxiety.
COIs overlap with cognitive and behavioral coping strategies. One of the most pervasive conclusions was the use of RRBs as a coping mechanism to alleviate anxiety as a product of sensory hyperresponsiveness (Gillott & Standen, 2007; Halim, Richdale, & Uljarević,