Gender differences in sensory sensitivity in ASD patients aged 2 to 15

doi:10.21203/rs.3.rs-3132801/v1

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Gender differences in sensory sensitivity in ASD patients aged 2 to 15

https://doi.org/10.21203/rs.3.rs-3132801/v1

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Background

Despite the high prevalence of sensory processing difficulties in children with autism spectrum disorder (ASD), research with a focus on the sex differences in sensory processing is limited contributing to later diagnosis, referral, and interventions. This study aimed to assess the gender differences in sensory sensitivity in ASD children.

Methods

190 youth with ASD,(age range 2–15 years,131 male and 59 female) were assessed in the Iran Autism Association clinic. The proportions of sensitivity present in Tactile / Taste Smell / Movement/ Visual and Auditory items and also the TOTAL SCORE were analyzed as a binomial outcome and compared between females and males. Patients were divided into four age groups and sensitivity by age group plots also were analyzed.

Results

In taste smell sensitivity and visual auditory sensitivity higher scores (indicating higher sensitivity) were found in females compared to males. Although movement sensitivity in females at younger ages was less than in males, at older ages it has been found that females are more sensitive to movement.ASD females showed higher scores at tactile sensitivity than males at older ages, compared to younger ages between 9 to 11 years.

Conclusion

Sex differences in sensory sensitivity were observed in ASD children aged 2 to 15, with females being more sensitive to ST/VA than males. On the other hand in total score and movement sensitivity, females got more scores at older ages. These findings reinforce the need to take a developmental approach to understand sex differences which may have diagnostic, prognostic and treatment implications.

autism spectrum disorder (ASD)

gender differences

sensory sensitivity

child development

sensory processing

short sensory profile-2(SSP-2)

Autism spectrum disorder (ASD) is a common neurodevelopment condition that is characterized by early-onset and persistent difficulties in social communication, sensory processing, and interaction along with repetitive or stereotyped behaviors. (1). The prevalence of ASDs was reported to be 2.64% (95% CI = 1.91–3.37), with 1.89% (95% CI = 1.43–2.36) in the general-population sample from regular schools and 0.75% (95% CI = 0.58–0.93) in the high-possibility group from special education schools and a disability registry. (2). Despite the heterogeneity in the manifestation and intensity of symptoms which lead to the identification of autism as a ‘spectrum’, it is widely reported to affect males(3,4)

1.1.Sex-bias, sex differences, and under-recognition of autistic females

Generally, males have been reported to be diagnosed four to five times more frequently than females; however, a systematic review and meta-analysis study suggests lower male-to-female ratios that are closer to 3:1 as females who would meet the criteria for autism may be at disproportionate risk of not receiving a clinical diagnosis. (5) Several possibilities can lead to the under-recognition of autistic females.

First of all, females may present with partly different behavioral characteristics (6,7,8)that make it more complicated for the autism phenotype to be recognized, diagnosed, and supported in an accurate and timely manner. (9)In addition to different behavioral characteristics, clinically diagnosed autistic females often present with coexisting emotional, behavioral, or cognitive difficulties including low intellectual level (10,11)and higher rates of co-occurring medical conditions, including epilepsy in comparison to autistic males. (6)As researchers often screen their participants to maximize the signal-to-noise ratio, females are more likely to be excluded from research due to the higher frequency of co-occurring conditions like epilepsy. As a result, Autism research studies have been dominated by male participants. So the male-to-female participant ratio in research is even more exaggerated compared to the general population prevalence ratio and it could limit the statistical power to detect small to moderate effects

.(12)The outcome of this condition would be a ‘male-based’ understanding of autism(13)

Furthermore, although hiding ASD symptoms or using compensatory behaviors to mitigate social challenges including reducing repetitive behavior, ‘stimming’ or responses to sensory over-stimulation has been reported in both gender(14,15,16,17), it is more common in females than males due to lack of impaired neural self-representation and mentalizing (18).

Considering these differences and a higher probability of hiding symptoms in females, it is necessary to conduct more investigations on the differences between females and males with ASD to reduce Sex-bias and under-recognition and reach an early diagnosis.

1.2. Sensory Processing, Sensory Over -Responsivity (SOR), Under-responsivity (SUR), and Sensory Seeking in ASD

Sensory processing refers to the way we sense, perceive, and respond to sensory stimuli present in the environment. This process is frequently referred to as a cascade that can be affected at different levels for instance, how incoming information is detected, how it is processed and integrated into the brain and, finally, how the ensuing behavior or response is modulated(19,20,21,22,23)Sensory processing disorders (SPD) are diagnosed when a patient presents with significant difficulties or abnormalities in detecting, modulating, interpreting or responding to sensory inputs(22)There are several methods for categorizing SPD. The most common is a scheme based on sensory modulation patterns: hypo-responsiveness, which refers to delayed responses or unresponsiveness to sensory stimuli; hyper-responsiveness, which is an exaggerated or even aversive reaction to sensory stimuli; and sensory seeking, which refers to an unusual fascination with the craving of sensory stimulation, often repetitive in nature (24,25,26,27,22,28)It has been reported that over 96% of children with autism suffer from Sensory Processing Disorder in one or multiple domains. These sensory behavioral problems range from mild to severe as well as communication and social deficits and can endure through adulthood. (29,30)Despite its prevalence (over 96%) and its impact on functioning in daily and social life, little has been said about sex differences in sensory processing in ASD and it is determined as one of the areas of ASD symptomatology which has suffered by lack of studies on sex differences which could further drive the male-biased knowledge base.

While a recent meta-analysis by Ben-Sasson et al. on sensory symptoms in ASD, it is not reported ‘Gender’ as a significant moderator in sensory processing disorders(31), Kumazaki et al. (32)reported higher scores in female children on “taste, smell and touch response,” compared to their male counterparts using the childhood autism rating scale.(CARS; 33)

In a study by Osório et al.(34) children aged 2 to 12 and 11 months have been studied in sensory processing, social participation, and praxis by using SPM(35,36)and SPM-Preschool (SPM-P,37,38) questionaries. The results of this study suggest that ASD females might be more likely to avoid or to be distressed by some auditory stimuli, to retreat from noisy environments, or to be distracted by sounds that others do not notice. Differences in the Balance and Motion subscale suggest that females may have more difficulties with movement coordination and postural control. Furthermore, females may have more difficulties in processing and responding to tactile stimuli, even though their results show only a slight trend. (34)

The results from these studies made our team eager to evaluate the sensory profiles of females and males by using more sensory instruments including short sensory profiles. This study aims to study sex differences in sensory sensitivity in ASD children. For this purpose, we short sensory profile-2 (DUNN-2014)(39).

The Sensory Profile 2 (Dunn, 2014) is a set of norm-referenced, parent and teacher questionnaires designed to assess the sensory processing patterns of children from birth through 14 years, and 11 months. There are five different forms selected based on age: 1) Infant Sensory Profile 2 – Birth to 6 months; 2) Toddler Sensory Profile – 7 to 35 months; 3) Child Sensory Profile 2–3 to 15 years; 4) Short Sensory Profile 2–3 to 15 years; and 5) School Companion Sensory Profile 2–3 to 15 years. (39)In this study we use short sensory profile-2 to evaluate children aged 2 to 14 and 11 months in Iran Autism Association.

2.1. Ethics Statement

Informed written consent was obtained for all participant's legal guardians by procedures approved by the Iran University Of Medical Science Ethics Committee.

2.2. Participants:

A total of 190 children were included in the analyses. Participants were recruited via research registries at the Iran Autism Association. Registry participants are referred through Autism Check-up Project, association clinics, and advocacy organizations to provide services for individuals with ASD. To acquire a sufficient sample of female children with ASD, families traveled from across the country to participate in this study.

Children were eligible to take part in the study if they met the following inclusion criteria:(1) diagnosed with ASD by a certified professional (psychiatrist, clinical psychologist)(2) aged between 2 and 14 years 11 months;(3) without an intellectual disability, as indicated by having an IQ above 70. (5) no other comorbidity like epilepsy and acute medical or genetic conditions(4) living in Iran. Under these criteria, 190 ASD participants (131 males, and 59 females )have been chosen to participate in this study.

2.3. Measures:

In this study, parents or legal guardians responded to caregiver-report questionnaires(SSP-2). The SSP-2 contains is a shortened form of Dunn’s Sensory Profile caregiver questionnaire which has 38 items organized into seven sub-scales: Tactile Sensitivity (TAC; 7 items), Taste/Smell Sensitivity (TSM; 4 items), Movement Sensitivity (MOV; 3 items), Under responsive/Seeks Sensation (USS; 7 items), Auditory Filtering (AFL; 6 items), Low Energy/Weak (LEW; 6 items), and Visual/Auditory Sensitivity (VAS; 5 items). These subs-scales represent observable child behaviors that are scored on a 1–5 rating scale based on their frequency (1 being “Always” and 5 being “Never”). The score on each sub-scale and Total score can be used to classify children’s level of sensory abnormality (Typical, Probably Difference, or Definite Difference) based on score percentiles from a large normative sample of children without disabilities(40). Burns et al. reported the SSP was the second most utilized measure (28.0% of studies) after the full-length SP, after a systematic review of 93 studies assessing sensory processing in ASD.(41)The SSP has been used as the sensory phenotyping measure of choice in large-scale ASD projects such as the Autism Speak Autism Treatment Network(42)and the EU-AIMS Longitudinal European Autism Project(43). However the reliability of each sub-scale was assessed by calculating Cronbach’s alpha for the 117-child sample (α = 0.82– 0.89) which shows a large correlation between the unit-weighted sub-scale scores in the sample (mean reported r = 0.53, range 0.25–0.72; 44), Williams ZJ et al. reported Sub scale alpha and omega total values, based on commonly-cited recommendations for internal consistency reliability(45), all satisfactory (> 0.7) which were notably homogenous (> 0.9) in TSM and LEW (46). As the language of this questionnaire is English, we used the Persian version of Sensory Profile 2 which is the translated form of this questionnaire. Mirzakhani et al.(47) studied Internal Consistency and Item Analysis of the Persian Version of the Child Sensory Profile 2 in Vulnerable populations. In this study, the Discrimination index was satisfactory for all the items of the Child Sensory Profile-2. The values of Cronbach’s alpha ranged from 0.795–0.919 in typical children and 0.617–0.901 in autistic children, and 0.792–0.920 in children with learning disabilities. Based on this study, the Persian version of the Child Sensory Profile 2 is a valid (discrimination with vulnerable populations) and reliable (internal consistency) tool for assessing sensory processing. (47) Despite the high reliability and validity of Children Sensory Profile − 2 which includes 86 items, our team decided to use Short Sensory Profile-2 which includes 38 items from Children Sensory Profile-2.its reduced participant burden relative to lengthier surveys, widespread use in the ASD literature and easier use by an assistant in counseling sessions were the reasons behind selecting this questionnaire for our research project.

2.4. Statistical analyses:

First, Cronbach’s alpha was calculated to examine the internal consistency of the Persian versions of Short Sensory Profile 2. In the next step, by the idea we got from the Mahenderian et al.(48) study, as dichotomizing reduces the variability of parental expectation of appropriate frequency of the behaviors, we decided to transform SSP-2 item scores into dichotomous variables. This transformation could cause an increase in our confidence that a particular sensitivity is present or absent(48).To accomplish this, each sub-scales score was divided into the number of components of the item. Then scores less than 2.49 were converted to “0” (corresponding to the Absence of Sensitivity), and scores between 2.50 to 5 were converted to “1” (corresponding to the Presence of Sensitivity).

All analyses were performed using SAS 9.4 (2002–2010 by SAS Institute Inc., Cary NC, USA ) and Minitab. we compared females and males in each sub-scale based on Data Means. Because the concept of p has no meaning here as we have to consider the values with the expected value, and we have no meaning for age here. That's why the mean is the best criterion for evaluating differences. we reported the result of 4 sub-scales (TAC, TSM, MOV, VAS) and also the SSP-2 Total Score. We also examined the sensitivity across ages in males and females by plots that showed scores in each age group. To accomplish this, we divided participants into 4 age groups due to having the same participants in each age group. Age groups include 1) 2 to 4;2) 5 to 8 ;3) 9 to 11; 4)12 to 15.

3.1. Study sample:

A total of 190 children from age 2 to 15 (131 (69%) male and 59 (31%) female ) were included in the analyses. Sample information and demographics are reported in Table 1. The internal consistency estimates for each sub-scale and questionnaire were reported in Table 2. The internal consistency of the sub-scales that we analyzed was above 0.70 and for the SSP-2 questionnaire was above 0.855 which shows acceptable reliability estimates.

Table 1

Baseline characteristics example
Characteristics
Number of participants	190
Age	9.67 ± 0.52
Gender
Male	131 (69%)
Female	59 (31%)

Table 2

Short Sensory profile-2 Internal consistency estimates (Crohnbach's alpha)
	Number of Items	Crohnbach’s alpha
-SSP2	38	0.855
Tactile Sensitivity	7	0.718
Smell Taste Sensitivity	4	0.889
Movement Sensitivity	3	0.857
Avoiding And Seeking	7	0.601
Auditory Filtering	6	0.678
Energy	6	0.898
Visual Auditory Sensitivity	5	0.791

3.2. Sex differences in TAC, TSM, MOV, VAS, and Total Score:

Tactile Sensitivity:

The result of analyzing females and males in Tactile Sensitivity are presented in Table 3. When comparing female and male participants in Tactile Sensitivity, males had significantly higher scores than females at younger ages. (age group 2–4)whereas females have been reported notably more sensitive to tactile sensation in ages 9–11. On the other hand, the pattern of sensitivity to age group, illustrates a rise in men’s tactile sensitivity in older ages (12–15), while females were less sensitive after age 11.

Taste Smell Sensitivity:

Based on the results (Table 4), in all age groups, females are more sensitive to Taste and Smell in comparison to males and there was a significant difference in the effect of age between 9 to 11 years old. Furthermore, in both gender, from the age of 2–4 to 5–8, children are getting more sensitive to Taste and Smell and it reaches to its peak at 5–8 years old. Then the sensitivity to taste and smell tends to decrease when they were getting older( after age 9 years old to 15)

Movement Sensitivity :

The result of analyzing females and males in Movement Sensitivity are presented in Table 5. Among both genders with ASD, Older children obtained higher scores in motion sensitivity than younger children. In younger age groups (2–8) males were reported to be more sensitive than females, whereas, in groups older than 9 years, females were reported to be more sensitive than males. The differences between males and females reach their peak at age 9–11 females are more motion sensitive approximately two times more than males. Both sexes have been more sensitive across age, but the magnitude was greater in females.

Visual/Auditory Sensitivity:

Table 6 represents the result of analyzing females and males in Motion Sensitivity. Although females have been reported to be more sensitive in all age groups, the differences between females and males were remarkably seen in younger ages. (age group 2–4). The pattern of sensitivity to the age group was similar between both genders and it showed a peak at 5 to 8 years old and a decrease in Visual/Auditory sensitivity after 8 years old.

Average Total Score:

Table 7 represents the result of analyzing females and males in Total items including seek and avoid, energy, auditory filtering in addition to sensory sensitivity items. In total scores, males have been reported to get higher scores at younger ages whereas females got higher scores than males after age 4.

In this study, we found that there were differences between females and males in sensory sensitivity. Females have been reported as more sensitive to Smell/Taste and Visual/Auditory Sensitivity. In addition, considering age's effect on sensory sensitivity, females are more sensitive to Motion and Tactile Sensitivity at older ages. This finding highlights the critical importance of examining age effects when exploring diagnostic group differences in behavioral, functional, and Sensory Processing Disorders (SPD) across ASD. we also assessed the internal consistency of the Persian version of Short Sensory Profile 2 which showed it is highly reliable.

Several reasons were suggested for differences in sensory sensitivity. One of the reasons could be differences in brain patterns in females and males. To investigate whether sex differences in the behavioral phenotype of ASD are linked to normative sex differences in brain neuroanatomy, Supekar k and Menon V. explored the relationship between the multivoxel brain morphometry patterns and symptom severity in girls and boys with ASD. Their findings indicate that the brains of girls with ASD are structured differently from those of boys which are linked to sex differences in behavioral impairments like lower severity of repetitive/restricted behaviors in girls. By using MVPA analysis, they found that the GM in several cortical and subcortical regions could differentiate girls and boys with ASD. GM volume in the left motor cortex, left supplementary motor area (SMA), left lingual/fusiform gyrus, left angular gyrus, right insula, bilateral cerebellum, and bilateral amygdala (height p < 0.001, FWE corrected, extent p < 0.01) notably showed high accuracies (85–90%) for distinguishing girls from boys with ASD. This study showed a classification accuracy of 88 percent for the left lingual/fusiform gyrus which is generally responsible for the higher processing of visual information. (49)

Later, Supekar k et al. studied one of the largest functional brain imaging cohorts of females and males with ASD, by using a novel spatiotemporal deep neural network ( stDNN ) model. It has been proved that brain features associated with motor, language, and visuospatial attentional systems reliably distinguish females with ASD from males and are contributing to their clinical symptoms in distinct ways. (50)

Ethical Approval:

The authors also would like to thank IAS Board’s members for granting the Autism Check-Up Project which helped our team to involve more participants and create an Autism Friendly Network that includes hundreds of clinics around the country to provide therapy for sensory problems.

Competing Interests:

The authors have no conflicts of interest to disclose.

Author’s contributions:

Dr.Alizadeh and Dr.Amiri conceptualized and designed the study, conducted and oversaw the review of abstracts and papers, drafted the initial manuscript, and reviewed and revised the manuscript. Mr.Miri and Dr.Tavakoli conducted background literature searches, wrote portions of the manuscript, reviewed abstracts and papers, and reviewed and revised the manuscript. Dr. Shirdel did the data analyzing, wrote portions of the manuscript and handled final submission processes .All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

Funding:

This work was funded by Iran Autism Association, Tehran.IAS is an NGO that provides supports, and financial aid and accelerates research in autism.

Availability of data and materials:

Anonymized data and materials are available upon request via the corresponding author.

All authors have read and approved the final manuscript. Our most sincere thanks go to all the caregivers, participants, and professionals of the Iran Autism Association, who helped us distribute the survey.

Ethical Approval:

Competing Interests:

The authors have no conflicts of interest to disclose.

Author’s contributions:

Funding:

This work was funded by Iran Autism Association, Tehran.IAS is an NGO that provides supports, and financial aid and accelerates research in autism.

Availability of data and materials:

Anonymized data and materials are available upon request via the corresponding author.

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Tables 3 to 7 are available in the Supplementary Files section.

No competing interests reported.

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Gender differences in sensory sensitivity in ASD patients aged 2 to 15

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Abstract

Background

Methods

Results

Conclusion

1. Introduction

1.1.Sex-bias, sex differences, and under-recognition of autistic females

1.2. Sensory Processing, Sensory Over -Responsivity (SOR), Under-responsivity (SUR), and Sensory Seeking in ASD

2. Method

2.1. Ethics Statement

2.2. Participants:

2.3. Measures:

2.4. Statistical analyses:

3. Result

3.1. Study sample:

3.2. Sex differences in TAC, TSM, MOV, VAS, and Total Score:

4. Discussion

5. Limitations and Future Directions

Declarations

References

Tables

Additional Declarations

Supplementary Files

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