Introduction
Autism spectrum disorder (ASD) is a neurodevelopmental condition characterized by two main features: persistent difficulties in social communication and social interaction as well as restrictive and repetitive patterns of behavior and interests.1–Reference Lai, Lombardo and Baron-Cohen4 Research in the field of ASD has been mainly focused on child samples, being the onset of the disorder typically in early life years.Reference Billeci, Calderoni and Conti2–Reference Lai, Lombardo and Baron-Cohen4 However, more recently, increasing attention has been paid on adult forms of ASD, with a specific interest on evaluating those milder forms, without intellectual disability or language development alterations, which may reach clinical attention only in adulthood when developing other disorders in comorbidity.Reference Lai, Lombardo and Baron-Cohen4–Reference Dell’Osso and Carpita7 In addition, the current scientific literature is also stressing the importance of identifying subthreshold manifestations of ASD, such as autistic traits (ATs), due to their possible impact on quality of life and their role as a vulnerability factor for the development of other psychiatric conditions.Reference Dell’Osso, Luche and Gesi5–Reference Dell’Osso and Carpita7 This kind of subthreshold manifestations, such as impaired social and communication skills, unusual and aloof personality, and repetitive and stereotyped behaviors, was originally detected among first-degree relatives of ASD probands, where they have been labeled as “broad autism phenotype.”Reference Billeci, Calderoni and Conti2, Reference Dell’Osso, Dalle Luche and Maj6, Reference Losh, Childress, Lam and Piven8–Reference Dawson, Estes and Munson12 However, further studies highlighted how AT seem to be continually distributed in the population, being particularly high in specific high-risk groups, such as university students of scientific coursesReference Choteau, Raynal, Goutaudier and Chabrol13–Reference Tchanturia, Smith and Weineck18 or clinical groups of psychiatric patients with other kinds of mental disorders.Reference Suzuki, Miyaki, Eguchi and Tsutsumi17–Reference Dell’Osso, Conversano and Corsi22 In this framework, it has been noted how both ASD and AT seem to play a significant role as vulnerability factors for the development of different psychiatric conditions, with a wide range of comorbidities between autism spectrum and several mental disorders.Reference Dell’Osso, Cremone and Amatori20–Reference Dell’Osso, Cremone and Carpita30 In this framework, a certain number of studies also reported a correlation between autism spectrum and trauma/stress-related symptoms.Reference Dell’Osso, Conversano and Corsi22 Some authors reported a post-traumatic stress disorder (PTSD) prevalence in children with ASD of approximately 67%, suggesting that these patients may be considered as a low resilient group with a greater vulnerability to the development of trauma and stress disorders.Reference Dell’Osso, Conversano and Corsi22, Reference Stavropoulos, Bolourian and Blacher31–Reference Roberts, Koenen, Lyall, Robinson and Weisskopf37 However, some data differ from those listed above, reporting lower prevalence rates between autism and PTSD.Reference Stavropoulos, Bolourian and Blacher31 The controversial reports about the association between ASD and PTSD has been hypothesized to be underlain by the fact that often ASD subjects are not able to properly mentalize and communicate eventual traumatic event.Reference Stavropoulos, Bolourian and Blacher31, Reference King38, Reference Dell’Osso, Abelli and Pini39 Individuals in the autism spectrum typically show difficulties in verbal and nonverbal communication with consequent problems in externalizing emotions, seeking help and adapting to stressful events.Reference Dell’Osso, Conversano and Corsi22, Reference Dell’Osso, Abelli and Pini40–Reference Motlani, Motlani and Thool43 On the other hand, the inflexibility and prowess toward rumination may facilitate the development of post-traumatic symptoms such as hyperarousal, intrusive thoughts, and re-experiencing.Reference Dell’Osso, Conversano and Corsi22, Reference Dell’Osso, Abelli and Pini40–Reference Dell’Osso, Lorenzi and Carpita42, Reference Ehlers and Clark44, Reference Kitamura, Makinodan and Matsuoka45
Some authors also suggested that these autistic features may easily lead to an inability to successfully cope not only with major traumatic events but also with minor events, the so-called microtraumas, developing chronic post-traumatic symptoms.Reference Dell’Osso, Conversano and Corsi22, Reference Dell’Osso, Abelli and Pini40–Reference Dell’Osso, Lorenzi and Carpita42 According to the concept of PTSD complex (cPTSD), the development of post-traumatic symptoms following prolonged and/or repeated mild traumatic events may be more frequent in vulnerable subjects and characterized by a greater tendency to chronicization, higher rates of dissociative symptoms, maladaptive behaviors, emotional dysregulation, and negative self-perception.Reference Dell’Osso, Conversano and Corsi22, Reference Carpita, Muti and Muscarella41, Reference Dell’Osso, Lorenzi and Carpita42, Reference Terr46–Reference Maercker, Brewin and Bryant52 It is also interesting to highlight that while, according to literature, ASD seems to be more prevalent among males,Reference Dell’Osso, Gesi and Massimetti14, Reference Baron-Cohen53 PTSD is more frequent in females.Reference Carmassi, Akiskal and Yong54–Reference Carmassi, Corsi and Bertelloni56 These data should be considered in light of recent studies suggesting a possible under-recognition of ASD among females due to gender difference in the presentation of the disorder, including a better ability in female patients to camouflage social difficulties by imitation strategies. As a consequence, autism spectrum among females may remain masked by other diagnosis, spanning from eating disorder to social anxiety, borderline personality disorders, and trauma and stress-related disorders.Reference Dell’Osso and Carpita7, Reference Dell’Osso, Gesi and Massimetti14, Reference Baron-Cohen, Cassidy and Auyeung57–Reference Marazziti, Abelli and Baroni59 Other studies also stressed that individuals with AT after traumatic exposure may more likely develop mood disorders, enhanced by PTSD symptoms and altered circadian rhythms symptoms. This hypothesis is in line with previous researches that highlighted a role of trauma/stress-related symptoms in the relationship between autism spectrum and increased suicidal risk.Reference Takara and Kondo19, Reference Kato, Mikami and Akama60 A previous study from Dell’Osso et al.Reference Dell’Osso, Conversano and Corsi22 also reported that, among university students, the presence of AT plays a role in the development of mood symptoms both directly and indirectly, through a mediating effect of trauma/stress-related symptoms. Furthermore, the authors suggested that traumatic experiences and the subsequent development of PTSD-like symptoms may on the development of mood condition. Finally, it is important to underline that, according to our vision, PTSD would not represent the end point of the disease pathway but the first step of a psychopathology trajectory that, starting from a neurodevelopmental impairment, may evolve toward mood disorders and catatonia, another condition often associated with both autism spectrum and PTSD.Reference Dell’Osso, Lorenzi and Carpita42, Reference Dell’Osso, Toschi, Amatori and Gesi61–Reference Dell’Osso, Amatori and Cappelli63
Our main hypothesis is that there is a correlation between elevated AT and post-traumatic stress symptoms and that, in this relationship, some symptom domains of autism, such as ruminative thinking and altered responsiveness to sensory stimuli, may play an important role.
Thus, the main aim of this study was to evaluate, in a sample of adults with significant AT and healthy controls (HCs), the relationship between autism symptoms and PTSD. The secondary aim was to investigate which specific autism dimension was more associated with trauma and stress-related symptoms in this population and eventually statistically predictive of developing PTSD.
Methods
Participants
We recruited a sample of 132 adult subjects without intellectual impairment or language development alteration who were addressed at the university psychiatric department. The recruitment period lasted from May 2015 to April 2017. The sample was divided in two groups: 68 subjects diagnosed with ASD according to the fifth edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-5) and scored above the cutoff for significant AT on the Adult Autism Subthreshold Spectrum (AdAS Spectrum) questionnaire (Autism Spectrum group). The second group was composed of 64 HCs who did not meet any criteria for ASD and scored below the threshold for significant AT on the AdAS Spectrum. All participants were assessed by trained clinicians according to DSM-5 criteria. All subjects received clear information about the study and had the opportunity to ask questions before providing a written informed consent. The study was led in accordance with the Declaration of Helsinki and approved by the Institutional Ethics Committee of Azienda Ospedaliero Universitaria Pisana (protocol code: 2015551).
Psychometric scales
All subjects were assessed with the AdAS Spectrum questionnaire and with the Trauma and Loss Spectrum (TALS) questionnaire, self-report version.
AdAS Spectrum
The AdAS Spectrum is a self-report instrument developed and validated in order to assess the wide range of subthreshold and full-threshold ASD manifestations among adults without intellectual disability or delayed language development. The questionnaire features 161 items with dichotomous answers (yes/no) divided into the seven domains: Childhood/adolescence, Verbal communication, Non-Verbal communication, Empathy, Inflexibility and adherence to routine, Restricted interests and rumination, and Hyper-hypo reactivity to sensory input. In the validation study, the AdAS Spectrum demonstrated good reliability and internal consistency, with Kuder–Richardson coefficients above 0.964. Also, in the sample of the present study, the AdAS Spectrum showed an excellent internal consistency (0.970). Although the AdAS Spectrum have been developed mainly as a qualitative and dimensional tool, it can also be use in a quantitative way, with a threshold of 43 for identifying significant AT and a threshold of 70 suggesting the presence of possibly clinically relevant ASD.Reference Dell’Osso, Gesi and Massimetti14, Reference Dell’Osso, Carmassi and Cremone64
Trauma and Loss Spectrum, Self-Report
The Trauma and Loss Spectrum, Self-Report (TALS-SR) is a self-report questionnaire with the aim to assess the broad range of symptoms related to stress, trauma, and loss in a dimensional fashion, evaluating the presence of a full-blown clinical picture as well as subthreshold or atypical symptoms across lifetime. The instrument features 116 items with a dichotomous answer (yes/no) organized in nine domains. According to the validation study, the instrument showed a good internal consistency and reliability.Reference Dell’Osso, Carmassi and Rucci65 Even in the sample of the present study, the TALS-SR showed an excellent internal consistency (0.970). Following the procedure described in previous studies, the TALS-SR can also be used for assessing the fulfillment of DSM-5 symptomatological criteria for PTSD (criteria B-E) on the basis of matched TALS-SR items.Reference Carmassi, Gesi and Simoncini66
Statistical analysis
We performed Mann–Whitney U test in order to compare mean age and scores obtained on the TALS-SR among groups. Chi-square tests were used in order to compare sex composition among groups as well as the presence or absence of a probable diagnosis of PTSD according to the TALS-SR. Spearman correlation coefficients were used for evaluating the association between AdAS Spectrum and TALS-SR scores in the whole sample. The sample size ensures 88.3% power for an α = 0.05 when comparing total TALS-SR scores between groups and 97.7% for an α = 0.05 when calculating correlations between total AdAS Spectrum and TALS-SR scores in the total sample. Furthermore, in order to identify the best predictors of the presence of a probable PTSD according to the TALS-SR, a first stepwise logistic regression analysis was performed with AdAS Spectrum total score as independent variable, followed by a second logistic regression analysis with AdAS Spectrum domain scores as independent variables to identify noteworthy predictors of PTSD symptomatology within the AdAS Spectrum domains and to quantify the extent to which the average risk of PTSD escalates with each one-point increase in AdAS Spectrum scores.
Results
The sample was composed of 83 males and 49 females. The mean age of the sample was 25.33 ± 0.73. No significant difference was reported among groups with respect to sex composition and mean age (see Table 1). The Autism Spectrum group reported a mean AdAS Spectrum total score of 76.09 ± 22.56, while HCs reported a mean score of 22.83 ± 11.50 (t = −17.23; p < .001). Subjects in the Autism Spectrum group reported a 30% rate of probable PTSD diagnosis according to TALS-SR, while no subjects in the HCs reported a PTSD diagnosis (see Table 2). Moreover, participants in the Autism Spectrum group also reported significantly higher scores on TALS total and domain scores when compared with HCs (see Table 3). Significantly positive and medium to strong correlations were reported between AdAS Spectrum and TALS-SR scores in the whole sample (see Table 4). According to the first logistic regression analysis, AdAS Spectrum total scores were reported to be statistically predictive of the presence of a probable PTSD diagnosis based on TALS-SR (see Table 5). The second logistic regression analysis, performed with a forward stepwise model including all AdAS Spectrum domain scores as independent variables, identified the AdAS Spectrum Hyper-Hyporeactivity to sensory input (step 1 and 2) and the Restrictive interest and rumination (steps 2 and 3) domains as positive predictors of a probable PTSD diagnosis based on TALS-SR (see Table 6).
Comparison of Sociodemographic Variables Between Groups
Differences in Prevalence Rates of a Probable Diagnosis of PTSD According to TALS-SR Between Groups
Comparison of TALS-SR Total and Domain Scores Among Groups
Spearman Correlations Between AdAS Spectrum and TALS-SR Scores in the Whole Sample
** p ≤ .001.
* p < .01.
Logistic Regression Analysis with AdAS Spectrum Total Score as Independent Variable and Presence/Absence of a Probable Diagnosis of PTSD Based on TALS-SR as Dependent Variable
Logistic Regression Analysis with AdAS Spectrum Domain Scores as Independent Variables and Presence/Absence of a Probable Diagnosis of PTSD as Dependent Variable
R 2 (Cox/Smell) = 0.229; R 2 (Nagelkerke) = 0.393; correct classification total percentage = 85.6%.
Discussion
The main aim of this study was to evaluate, in a sample of adults, whether the presence of PTSD spectrum symptoms was associated with autism spectrum, also evaluating which autism spectrum dimension may be more associated with trauma/stress-related symptoms and statistically predictive of PTSD clinical picture. In order to assess the presence of PTSD full-fledged symptoms, we chose to refer only on symptomatological criteria (B-E), as assessed by the TALS-SR excluding the criterion A (which assess the presence of critical traumatic experiences). This choice was made in light of the rising cPTSD model, according to which vulnerable subjects may develop a PTSD condition also after minor traumatic events not included in criterion A, especially if prolonged or repeated in time.Reference Dell’Osso, Conversano and Corsi22, Reference Dell’Osso, Abelli and Pini40, Reference Carpita, Muti and Muscarella41, Reference Motlani, Motlani and Thool43, Reference Kitamura, Makinodan and Matsuoka45–Reference Dell’Osso, Lorenzi and Carpita50 In addition, subjects in the autism spectrum, even when having experienced major traumatic events, may not be able to properly report it due to their difficulties in processing and communicating life experiences.Reference Dell’Osso, Luche and Gesi5, Reference Dell’Osso and Carpita7, Reference Stavropoulos, Bolourian and Blacher31, Reference Van der Kolk48 According to our findings, autism spectrum subjects reported a strikingly higher rate of PTSD when compared with the HC group from our study (30% versus 0%). The reported prevalence was higher also when compared with ranges reported in the general population, which are around 3–4%.1, Reference Javidi and Yadollahie67–Reference Christiansen and Berke70 On the other hand, the absence of cases among HCs, with a consequent prevalence rate likely lower to that reported in general population samples, may also be ascribed to the fact that participants in the HC group were specifically selected among people without significant subthreshold AT, which are instead continuously distributed in the general population.
This finding was further supported also by the significantly higher scores reported on all TALS-SR domains by autism spectrum subjects than HCs. Our data are in line with studies reporting an increased prevalence of PTSD symptoms among subjects diagnosed with ASD or with higher AT,Reference Dell’Osso, Conversano and Corsi22, Reference Stavropoulos, Bolourian and Blacher31–Reference Roberts, Koenen, Lyall, Robinson and Weisskopf37, Reference Carpita, Muti and Muscarella41, Reference Dell’Osso, Lorenzi and Carpita42, Reference Van der Kolk48, Reference Baron-Cohen, Cassidy and Auyeung57, Reference Lai, Baron-Cohen and Buxbaum58, Reference Dell’Osso, Toschi, Amatori and Gesi61, Reference Golan, Haruvi-Lamdan, Laor and Horesh71 eventually supporting the hypothesis that ASD may act like a factor of vulnerability for developing symptoms after traumatic events.Reference Dell’Osso, Conversano and Corsi22, Reference Stavropoulos, Bolourian and Blacher31, Reference Dell’Osso, Lorenzi and Carpita42, Reference Baron-Cohen, Cassidy and Auyeung57, Reference Lai, Baron-Cohen and Buxbaum58, Reference Dell’Osso, Amatori and Massimetti62, Reference Dell’Osso, Amatori and Cappelli63 In particular, the presence of AT, which results in reduced coping strategies and difficulties in processing stressful experiences, may lead to an increased vulnerability to a wide range of trauma or stress-related symptom.Reference Dell’Osso, Conversano and Corsi22, Reference Dell’Osso, Lorenzi and Carpita42, Reference Ehlers and Clark44, Reference Baron-Cohen, Cassidy and Auyeung57, Reference Lai, Baron-Cohen and Buxbaum58, Reference Dell’Osso, Toschi, Amatori and Gesi61, Reference Dell’Osso, Amatori and Cappelli63 Considering that subjects with AT may have difficulties also in emotional expression and impairment in peer relationships, the lack of ability to request and obtain social support may enhance the negative impact of the stressors.Reference Dell’Osso, Conversano and Corsi22, Reference Carpita, Muti, Cremone, Fagiolini and Dell’Osso29, Reference Dell’Osso, Abelli and Pini39, Reference Dell’Osso, Lorenzi and Carpita42, Reference Baron-Cohen, Cassidy and Auyeung57, Reference Lai, Baron-Cohen and Buxbaum58, Reference Dell’Osso, Toschi, Amatori and Gesi61, Reference Dell’Osso, Amatori and Cappelli63 Noticeably, the autism spectrum group reported higher scores also on TALS domain, investigating the wide spectrum of loss events and potentially traumatic events. These domains do not assess only major traumatic or loss events but also minor ones for which the subject experienced distress (such as changes in home or school, school or work failures, etc.). While people with AT may be more frequently exposed to traumatic events, especially relational ones, due to their difficulties in understanding social clues, it is also possible that, if directly asked, they recall as distressing a wider range of events with respect to subjects without AT.Reference Dell’Osso, Dalle Luche and Maj6, Reference Dell’Osso, Conversano and Corsi22, Reference Kanne, Christ and Reiersen26, Reference Stavropoulos, Bolourian and Blacher31, Reference Dell’Osso, Lorenzi, Nardi, Carmassi and Carpita36, Reference Roberts, Koenen, Lyall, Robinson and Weisskopf37, Reference Dell’Osso, Lorenzi and Carpita42, Reference Van der Kolk48, Reference Baron-Cohen, Cassidy and Auyeung57, Reference Lai, Baron-Cohen and Buxbaum58, Reference Kato, Mikami and Akama60, Reference Dell’Osso, Amatori and Cappelli63, Reference Rumball, Happé and Grey72
According to our data, significant and positive correlations were found between AdAS Spectrum and TALS-SR scores, with the highest correlations reported between TALS-SR total score and AdAS Spectrum domains related to rumination, altered reactivity to sensory input, inflexibility, and adherence to routine. In addition, according to the regression analysis, in our sample, the AdAS Spectrum total scores were statistically predictive of the presence of a symptomatic diagnosis of PTSD. The AdAS spectrum domains significantly predictive of the presence of a PTSD clinical picture were Restrictive Interests and Rumination and, to a lesser extent, Hypo-Hyperreactivity to sensory input. These results are in line with the previous literature which stressed a significant role of ruminative thinking for the development of PTSD in subjects previously exposed to a trauma.Reference Dell’Osso, Conversano and Corsi22, Reference Dell’Osso, Abelli and Pini40, Reference Ehlers and Clark44, Reference Baron-Cohen, Cassidy and Auyeung57, Reference Lai, Baron-Cohen and Buxbaum58, Reference Dell’Osso, Amatori and Cappelli63, Reference Woodward, Sachschal, Beierl and Ehlers73, Reference Viana, Paulus and Garza74 In this framework, ruminative thinking may act both as a maintaining and exacerbating factor for PTSD.Reference Roley, Claycomb and Contractor75–Reference Olatunji and Wolitzky-Taylor77 On the other hand, the altered reactivity to sensory input may be considered as a further element of enhanced vulnerability to external events, which, together with inflexibility traits, may impair the ability to adjust to changes in the environment.Reference Dell’Osso, Dalle Luche and Maj6, Reference Dell’Osso, Conversano and Corsi22, Reference Dell’Osso, Lorenzi and Carpita50 In clinical terms, being aware of a correlation, as evidenced by scientific literature, between elevated AT and post-traumatic stress symptoms could assist clinicians in preventive efforts for individuals within the autism spectrum. This may involve primarily psychoeducational interventions aimed at reducing the likelihood that traumatic experiences encountered by these vulnerable individuals could lead to the development of full-fledged PTSD or complex PTSD. This study should be considered in light of some important limitations. First of all, it is impossible to identify the temporal relationship between AT and the appearance of stress and trauma-related symptoms due to the cross-sectional design of the study. Secondly, the investigated sample was relatively limited in number, limiting the extensibility of our results. Furthermore, we used self-reported questionnaires that may cause a hyper- or under-evaluation of symptoms by the subjects. In addition, we have to consider that the presence of PTSD may have influenced obtaining high scores at some AdAS domains such as altered responsiveness to sensory stimuli, especially considering the complex interaction between AT and post-traumatic symptoms in composite and still not formally categorized frameworks such as complex PTSD. Despite these limitations, globally, our study seems to confirm a strong correlation between autism spectrum and PTSD symptoms. Further studies should address the issue of stress/trauma-related disorders in this population, considering also that the development of a PTSD-like syndrome, if not properly recognized and treated, may facilitate the development of other disorders in comorbidity, worsening the illness trajectory of ASD.Reference Dell’Osso, Dalle Luche and Maj6, Reference Dell’Osso, Conversano and Corsi22, Reference Dell’Osso, Lorenzi and Carpita50
Conclusion
High rates of PTSD were found in subjects with significant AT. In particular, among the symptom dimensions of autism, ruminative thinking, restricted interests, and altered sensitivity to sensory stimuli were found to be predictive of the presence of a PTSD diagnosis.
Author contribution
Conceptualization: B.C., L.D.O.; Investigation: B.C., F.G., I.M.C., G.A.; Supervision: B.C., L.D.O.; Writing – review & editing: B.C., I.M.C., G.A.; Formal analysis: E.M.; Software: E.M.; Writing – original draft: F.G.; Data curation: G.A.
Financial support
This research received no specific grant from any funding agency, commercial, or not-for-profit sectors.
Competing interest
All authors declare that they have conducted the research without any financial, professional, contractual, or personal relationships that could be interpreted as a potential conflict of interest. The authors have nothing to disclose.
