Vocal and motor behaviors as a possible expression of gastrointestinal problems in preschoolers with Autism Spectrum Disorder

Autism spectrum disorders (ASD) are a group of neurodevelopmental disorders characterized by social and communication impairment along with the presence of repetitive and restrictive behaviors [1]. According to a recent Italian population study, the prevalence of ASD in children aged 7–9 years is of about one in 87 [2].

A number of co-occurring health conditions were described in ASD (for a recent systematic review see Muskens et al. [3]), contributing to the considerable ASD clinical variability, and impacting on quality of life both of the children and their parents [4]. Within the medical comorbidities, gastrointestinal (GI) problems are widely reported by several studies [5‐15], and among them constipation and diarrhea were the most commonly observed symptoms. Marked variation exists among studies on the prevalence of GI problems in ASD pediatric population, partly related to the different tools used for the GI assessment [15, 16]. Specifically, the prevalence is greater in investigations that include functional and idiopathic GI symptoms, and examine data from parents’ reports considering longer time intervals [17, 18] than in studies reporting organic GI diseases, clinician’s evaluation, or considering shorter time ranges. Moreover, Gorrindo et al. [19] reported that the majority of GI symptoms in children with ASD are due to functional causes.

More anxiety and sensory over-responsiveness [20], irritability [8], sleep problems [21], rigid-compulsive behaviors [13, 22], opposition and emotional dysregulation, as well as anxiety and affective disorders [23] were described in ASD subjects with GI impairment in comparison with ASD children without GI symptoms. Currently, there is a paucity of literature on differences in clinical manifestations between subjects with functional GI problems and subjects with organic GI problems [15].

Crucially, autism-related communication impairments may lead to unusual manifestations of GI disorders [24, 25]. In fact, many children with ASD have limited expressive language abilities as well as sensory processing impairments that could prevent the effective communication and/or the proper localization of pain of some GI symptoms [24, 26, 27]. Therefore, in ASD children clinical tools based on observable manifestations could be more useful than those based on reported symptoms.

Accordingly, in the ‘Consensus Report on the evaluation, diagnosis and treatment of GI disorders in ASD subjects’ [24] several behaviors (Verbal Behaviours “VB”, Motor Behaviours “MB” and Changes in Overall State “C”) that could be considered as alternative ways of expressing GI disorders in individuals unable to effectively communicate their discomfort are reported. The authors called all these behaviors “Associated Behaviors” (AB) [25].

Two studies [28, 29] tested AB in ASD children in order to determine if they occurred more frequently when a GI disorder was present. The first investigation evaluated 487 ASD children with and without GI problems and showed that unusual sleeping or eating habits as well as oppositional behaviors were significantly associated with GI problems [28]. In a subsequent study [29], the authors proposed a brief parent-report screen able to identify functional constipation, functional diarrhea, and gastroesophageal reflux disease (GERD) in ASD children, which minimally relied upon the child’s ability to report or to localize pain. This screening tool asked about the recurring motor acts described in the Consensus report [24] proving to be particularly useful for identifying cases of GERD.

The exploration of the association between GI symptoms and AB could allow to better identify the presence of GI problems, improving care and quality of life of ASD subjects.

Therefore, the main aims of our study are:

No statistically significant differences were found comparing males vs females for all variables, therefore the sample was considered as a unit. Thirty children (35%) were in the GI group, and 55 (65%) in the No-GI group. There were no significant differences in clinical variables between the GI and the No-GI groups, with the exception of the Global Score of the RBS-R, the Internalizing and Externalizing problem scores of the CBCL (all significantly higher in the GI group than in the No-GI group), and of the Communication and Daily Living adaptive scores of the VABS-II (significantly higher in the No-GI group than in the GI group) (see Table 2).

Therefore, we examined the correlations of the 6-GI scores with the ABQ Total Scores in the whole sample (R = 0.422, B = 1.394, p = < 0.001). In the multiple regression model, the correlation between the 6-GI scores and the ABQ Total Scores persisted even after correction for the variables that significantly differ between the GI and the No-GI group (p = 0.0026).

As far as the single AB is concerned, a positive correlation between the 6-GI scores and VB total score (p = 0.009), and with “frequent clearing of throat, swallowing and/or tics” (p = 0.043), “screaming” (p = 0.048), “sighing and/or whining” (p = 0.039), “moaning and/or groaning” (p = 0.003), and “direct verbalization about pain or stomach” (p = 0.015) scores was detected.

In addition, a positive correlation between the 6-GI scores and MB total score (p = 0.015), “facial grimacing” (p = 0.010), “constant eating/drinking/swallowing” (p = 0.002), “application of pressure to abdomen” (p = 0.032), and “aggressive behaviors” (p = 0.032) scores was observed.

The statistically significant correlations of the 6-GI scores with the three summary clusters (VB, MB and C) and with the singles items of the ABQ are reported in Table 3.

Thirty-nine participants (46%) were verbal and 46 (54%) were non-verbal. Among the 39 verbal subjects, 10 children (26%) were in the GI group, whereas among the 46 non-verbal subjects, 20 children (44%) were in the GI group. No statistically significant differences were found between verbal and non-verbal groups as far as the prevalence of GI subjects (p = 0.086), the 6GI scores and the Total GSI scores (Table 4).

We found significantly higher scores for the GI group on the “ABQ Total Score”, and in all the three ABQ cluster scores (Table 4). Furthermore, statistically significant higher mean scores were detected in the GI group than in the No-GI group in the following items: “sighing and/or whining”, “moaning and/or groaning”, “facial grimacing”, “constant eating/drinking/swallowing”, “application pressure to abdomen”, “tapping behaviors”, and “sleep disturbances”.

Three items of the ABQ were statistically significant higher in the non-verbal group than in the verbal group: “frequent clearing of throat, swallowing and/or tics”, “moaning and/or groaning”, “mouthing behaviors”.

Then, we examined the correlations between the 6-GI symptoms and the ABQ Total Score in the verbal group (R = 0.310, B = 1.246, p = 0.090) and in the non-verbal group (R = 0.481, B = 1.634. p = 0.006).

In the verbal group, the 6-GI Score was positively correlated with “frequent clearing of throat, swallowing and/or tics” (p = 0.022), “direct verbalization about pain or stomach” (p = 0.018), “constant eating/drinking/swallowing” (p = 0.007), and “sleep disturbances” (p = 0.014).

The statistically significant correlations between the 6-GI score and the 3 summary clusters (VB, MB and C) and with each AB of the verbal subjects are reported in Table 3.

In the non-verbal group, the 6-GI score was positively correlated with VB total score (p = 0.001), “screaming” (p = 0.005), “sighing and/or whining” (p = 0.031), “moaning and/or groaning” (p = 0.002), C total score (p = 0.021), and with “sleep disturbances” (p = 0.045).

The statistically significant correlations between the 6-GI score and the three summary clusters (VB, MB and C) as well as with each AB of the non-verbal subjects are reported in Table 3.

Finally, considering the possible influence of having more internalizing or more externalizing problems on the subject’s expression of abdominal discomfort, we analyzed the correlations between the CBCL scores (Internalizing, Externalizing, Total Problems) and the 6-GI scores. The Internalizing Problems and the Total Problems were significantly correlated with the 6-GI score (p = 0.006 R = 0.30, and p = 0.036 R = 0.23, respectively). We did not find significant correlation between the 6-GI scores and the Externalizing Problems.

Over the past years, the evaluation and the understanding of GI symptoms in ASD individuals are considerably improved, and crucially the importance of considering behavioral symptoms as a possible expression of GI distress is repeatedly emerging [13, 15, 19, 22, 28, 29].

To the best of our knowledge, this is the first study that seeks to investigate the possible association between all the AB and GI symptoms, with the aim of contributing to a better comprehension of the way by which ASD subjects signal the presence of a GI problem.

Results pointed out to significantly higher scores in ABQ Total scores as well as in the scores of the three clusters proposed by Buie and colleagues [24] in subjects with significant GI symptoms than in subjects without, with some AB significantly associated to the presence of an underlying GI problem. The abovementioned association was maintained independently from clinical variables -involving the adaptive functioning and emotional-behavioural psychopathology- that distinguish GI from No-GI subjects. These findings could provide a new interpretation for some events that are usually considered part of the autistic symptomatology [15, 45]. The sudden appearance of self- and other-directed aggression, an increase in motor activity or in repetitive behaviors and a worsening of global adaptive behaviors in ASD subjects could suggest clinicians starting or increasing a psychopharmacological treatment that instead could be prevented through a correct diagnosis and appropriate treatment of the underlying GI problem. Accordingly, the contribution of GI symptoms to the onset of sudden irritability or aggressive behavior in non-verbal ASD children has already been reported [28, 46]. In addition, we confirm our previous findings showing that ASD subjects with GI problems have a worse clinical functioning than ASD subjects without GI problems, independently from the severity of autistic symptoms [14]. Of note, the presence of more substantial internalizing or externalizing symptoms may influence the subject’s expression of abdominal discomfort.

Behaviors like sighing and/or whining, moaning and/or groaning, facial grimacing and sleep disturbances are easily associable to the discomfort of an underlying GI problem. Other manifestations like constant eating/drinking/swallowing, application pressure to abdomen and tapping behaviors are more difficult to predict in these subjects. Since the action of constantly eating small amounts of food or repetitively swallowing with a feeling of obstruction (dysphagia) are key symptoms of gastro-esophageal reflux (GER), we can hypothesize a link between “constant eating/drinking/swallowing” behavior and GER. This result could be particularly relevant, since GER is a problem difficult to identify in the early stage, which often leads to medical complications, and usually requires invasive diagnostic techniques [47]. “Holding the abdomen” has already been referred to constipation in children and adolescents with ASD [48], and it could be the only visible sign of a health issue with a high rate of hospitalization [49]. It has also been associated with GERD, intestinal inflammation, malabsorption and maldigestion [24, 29]. “Tapping behaviors” have been only recently considered as a possible expression of GI problems [24], since they were frequently interpreted as a behavior specific to autism [50]. In all these cases, the modalities of onset (e.g. sudden or gradual) and other anamnestic information are needed for symptom characterization and proper treatment options.

Previously, it has been suggested that the presence of these AB is not useful per se for the identification of GI problems, since they are very common also in children without GI problems [28]. Buie and colleagues [24] pointed out that the motor behaviors are not specific to GI problems, but may be indicative of pain or discomfort arising also in other parts of the body. Our study found a positive correlation between the 6-GI score and all the three ABQ clusters, showing for the first time a specificity of these behaviors. In particular, some specific behaviors seem to represent a direct expression of a GI problem in ASD subjects: vocal behaviors like “frequent clearing of throat, swallowing and/or tics”, “screaming”, “sighing and/or whining”, “moaning and/or groaning”, “direct verbalization about pain or stomach”, and motor behaviors like “facial grimacing”, “constant eating/drinking/swallowing”, “application of pressure to abdomen” and “aggressive behaviors”, as well as “changes in overall states”.

As far as the comparison between verbal and non-verbal children, the two groups showed several significant differences when the 6-GI Score was taken into account. “Mouthing behaviors” seemed to differentiate verbal from non-verbal subjects. “Frequent clearing of throat, swallowing and/or tics”, “direct verbalization about pain or stomach” and “constant eating/drinking/swallowing” are symptoms that characterized the verbal group with higher 6-GI scores, whereas “screaming”, “sighing and/or whining” and “moaning and/or groaning” were more representative for the non-verbal group with higher 6-GI scores. Notably, “sleep disturbances” were present in both groups, in agreement with previous literature [28, 51, 52]. Therefore, non-verbal subjects with a more relevant GI symptomatology show more frequently vocal behavior and changes in the global state than verbal subjects with a GI disturb. Interestingly, there were no significant differences in the prevalence and severity of GI symptoms between verbal and non-verbal subjects. In a recent review, the authors concluded that it was not possible to examine the association between GI symptoms and verbal skills in subjects with ASD, since the majority of studies did not distinguish the prevalence of GI symptoms on the basis of expressive language level (e. g. verbal vs non-verbal subjects). By evaluating the inverse relationship, previous investigations on relatively small samples detected both lower verbal abilities [19] and no differences of verbal skills [6, 53] in ASD children with GI problems compared to ASD children without GI problems. This result supports the view that non-verbal ASD children differ from verbal ASD patients only in the modalities of GI discomfort expression, but not in the prevalence or global intensity of GI symptoms. We can hypothesize that non-verbal children activate a minimally verbal behavior to report a physical discomfort (AB as “screaming”, “sighing and/or whining” and “moaning and/or groaning”), while verbal subjects more frequently verbalize their pain (AB as “direct verbalization about pain or stomach”). Importantly, the relatively low average age and the high proportion of subjects not-evaluable at the psychometric test (i.e. more functionally compromised) could partly explain the significantly higher presence of behaviors like “frequent clearing of throat, swallowing and/or tics” in verbal subjects, as well as the low prevalence of “delayed echolalia that includes reference to pain or stomach” in both groups and in the total sample. Crucially, this result indicates that verbal subjects with autism use direct verbalizations, rather than echolalia, to signal a discomfort.

It is important to be aware of the atypical presentation of GI symptoms [54]. Usually, the questionnaires that investigate the GI symptoms in ASD children are based almost exclusively on the symptoms reported by the parents rather than on the visible signs [6, 20, 52, 53, 55, 56].

The presence of significant GI symptoms has been evaluated through the administration of parent-report questionnaire and this could represent a limitation, particularly in younger subjects or in children with more severe autistic symptoms [15]. However, a high concordance between parental reports and gastroenterologist evaluations has been reported [19, 29].

In the future, the sensitivity and the specificity of our results could be enhanced by providing a complete gastroenterological evaluation in ASD subjects with higher GI total scores or at least in the positive cases [29]. Conversely, our protocol could be recommended in hospitals with limited economic resources.

The GSI does not evaluate the presence of some frequently reported GI symptoms, such as GER and vomiting and the cut-off we used was based on the examination of the previous literature, but it is not yet validated. Furthermore, a potential bias derived from the expected numerical disparity between GI and No-GI subjects may affect interpretation of results. Finally, our results are limited to functional GI disorders: therefore, additional research on the associated behaviors in children with organic GI problems is needed.

In addition, a future comparison between these results and those obtained from a group of age and sex matched typical controls could be useful in order to better understand the features of the AB related to the GI symptomatology, independently from an ASD diagnosis.

In summary, our results encourage researchers to adapt the current tools used to investigate GI symptomatology in ASD subjects, through the addition of items that are based also on objective measures. The evaluation of AB may be useful to identify the presence of GI problems in the ASD populations, and especially in non-verbal ASD children. Moreover, it is important to enhance clinicians’ awareness of the high co-occurrence of GI symptoms in ASD subjects, so that targeted investigations can be undertaken [45].

Our understanding of GI problems in ASD in relation with AB has come a long way, but further studies and more systematic research are warranted.