Sensory processing abilities and their impact on disease severity in children with attention-deficit hyperactivity disorder

INTRODUCTION

Attention-deficit/hyperactivity disorder (ADHD) is a neurodevelopmental disorder, which is as common as affecting around 7% of school-age children.^[1,2] The diagnostic criteria described in the Fifth Edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-V) are commonly used to diagnose ADHD and divide ADHD patients into three subtypes: Predominantly inattentive subtype (ADHD-I), predominantly hyperactive-impulsive (ADHD-HI), and combined subtype (ADHD-C).^[3] Apart from the core symptoms of impulsivity, hyperactivity, and inattention, ADHD patients often show several comorbidities such as conduct disorder (CD), oppositional defiant disorder (ODD), sleep disturbances, tics, learning disability, anxiety, and depression.^[4] However, sensory processing abnormalities are not considered either as a core feature or commonly associated with the comorbidity of these disorders.^[5] A few studies in the past two decades have explored the sensory processing abilities of ADHD patients from various parts of the world.^[6-8] Most of the completed studies showed at least some clinically/subclinically detectable hyporesponsivity/ hyperresponsivity to auditory, visual, and tactile stimuli.^[9,10] Second, previous studies have also shown that these sensory processing issues also affect the symptom profile and severity of ADHD.^[11,12] However, the systematic review by Ghanizadeh.^[5] could not reach at a definite conclusion due to the several methodological limitations and the small sample size of many included studies. We have planned to compare the sensory processing problems of ADHD patients with typically developing children using a standardized validated measure like sensory profile-2 (SP-2) and will evaluate for determinants and impact of sensory processing problems in these patients.

MATERIALS AND METHODS

This was a cross-sectional study conducted in a tertiary care hospital and associated medical college in North India between August 2019 and November 2022. The primary objective of this study was to compare the sensory responses of children and adolescents with and without ADHD aged 6–15 years. The secondary objectives were to describe the neurobehavioral profile and psychiatric and other comorbidities of ADHD patients and to correlate the sensory processing problems in these patients, with the symptom profile and severity of ADHD.

In the study by Shimizu et al.,^[13] a moderate effect size was observed for the difference in sensory responses of children with and without ADHD. Hence, we assumed the effect size for the difference in sensory responses between the two groups to be 0.5. With a presumed, power of 80%, alpha error of 0.05, and an allocation ratio of 2:1 in ADHD and control group, we calculated a sample size of 66 in ADHD group and 33 in the control group.

We included patients aged 6–15 years with ADHD satisfying DSM-V criteria for the same (ADHD-HI, ADHD-I, and ADHD-C subtypes), in the ADHD group. We attempted to include all consecutive children and adolescents satisfying the inclusion criteria to be included in the study, to avoid sampling bias, irrespective of the duration of illness, previous medications or behavioral therapy, or comorbidities. The participants in the control group were matched to the participants in the ADHD group, for three main sociodemographic variables (gender, age, and socioeconomic status [SES]) and without any major systemic illness. For matching, we started with a number “1” and then every alternative participant from the first participant in the ADHD group was matched for age, gender, and SES, to ensure a 2:1 enrolment ratio, without any bias.

After obtaining Institutional Ethics Committee approval and informed written consent from the caregivers, the participants were subjected to detailed clinical and neuropsychological examination, apart from noting their sociodemographic details. In clinical variables, we included any abnormalities on physical examination or neurological examination, previous history of seizure or other neurological problems, and any comorbid illnesses such as CD, ODD, sleep problems, specific learning disability (SLD), substance abuse, epilepsy, and autistic features. We also noted their recent most academic grades and whether they were studying to age-appropriate standards in school/ in the past required multiple attempts to pass a particular standard.

The neuropsychological assessment included the following: ADHD symptoms severity was rated by the revised Connor’s Parent Rating Scale-Revised (CPRS-R), intellectual level of the participant was tested using the Malin’s Intelligence Scale for Indian Children, presence, and severity of SLD were assessed by Grade Level Assessment Device and National Institute of Mental Health and NeuroSciences SLD battery. The attention was specifically assessed by the Continuous Performance Test, working memory was assessed by the forward and backward digit span test and Corsi Block-Tapping test, and executive function by the Behavior Rating Inventory of Executive Functions (BRIEF) test.^[14-16] Other comorbidities were initially screened with the Child Behavior Checklist, and subsequently, their diagnosis was confirmed with DSM-V criteria for individual disorders. The severity of comorbid ODD and CD were measured by the ODD Rating scale (ODDRS) and CD Rating Scale-for parents (CDRS-P), respectively, whereas comorbid depression severity was measured by CDRS.^[17,18]

Children in whom ADHD symptoms were not the primary concern and they were suffering mainly from other pervasive developmental disorders such as autism spectrum disorder or psychiatric disorders such as bipolar disorders, major depressive disorder, schizophrenia neurological disorders (e.g., cerebral palsy, epileptic encephalopathy, neurodegenerative disorder, and non-traumatic and traumatic brain injury), and intellectual disability (intelligence quotient <70) were excluded from the study.

Child SP-2 was used for assessing sensory processing abilities. It is answered by a parent or caregiver and the questions are designed to measure the behavioral responses of children to daily sensory events. It can detect both under-responsivity corresponding to a high neurological threshold and over-responsivity corresponding to a low neurological threshold.^[19]

This scale has 86 items, which are arranged into 14 sections, 4 response patterns, and 9 factors. Sensory processing, modulation, and behavioral and emotional responses are three categories, into which these 14 sections are divided into. Combined scores from different sections lead to 9 factors. The combined scores from these factors determine the four response patterns. A higher score indicates a lower frequency of undesirable behavioral responses to sensory stimuli. Separate investigators performed SP-2 and the rest of the other neuropsychological assessments, unaware of the findings of each other to avoid bias.^[20]

RESULTS

Out of the 66 ADHD patients enrolled (60 boys, 90%, 10.7 ± 1.9 years), 5, 19, and 42 cases were of the ADHD-I, ADHDHI, and ADHD-C types, respectively, according to DSM-V criteria. Fifty-four (83%) cases had at least one or more ADHD-associated comorbidity. SLD (n = 31, 46%), ODD (n = 37, 55%), CD (n = 22, 34%), anxiety (n = 17, 27%), depression (n = 9, 13%), somatic symptoms (n = 25, 39%), sleep problems (n = 23, 35%), motor/vocal tics (n = 16, 25%), and obsessive compulsion disorder (n = 5, 8%) were various comorbidities reported in our cohort. As high as 63 (96%) of participants were receiving at least one medication for ADHD, as in our center, we routinely prescribe both behavioral intervention and medications simultaneously, unless medications are not required clinically or contraindicated. While 34 (51%) participants were receiving atomoxetine alone, 22 (33%) and 2 (3%) children were receiving methylphenidate and clonidine. Rest, 5 (7.5%) children were receiving both methylphenidate and atomoxetine. The baseline demographic and clinical characteristics of the ADHD group and age, gender, and SES are shown in [Table 1].

The ADHD group had a significantly low raw score on most of the factors, sections, and response patterns of the SP-2 [Table 2]. The effect size for the difference between the two groups was moderate or large for ten out of 14 sections of the SP. However, none of the participants in either group had values suggesting that they are much more or much less likely as compared to the others in the general population. However, in the ADHD group, four and two participants had auditory and visual processing scores in the range suggesting that they are more likely to have auditory and visual processing problems compared to the majority of others, in contrast to the typically developing control group, who had scored for individual sections in the range, which suggested that they are behaving like the majority of others in the general population. Furthermore, the difference between the proportion of participants in ADHD and control groups who had scores for individual sections in the clinically abnormal range was not statistically significant (P > 0.05, for all).

When we compared the scores on various SP-2 subsections between three sub-types of ADHD, there were no significant differences between them, although there was a trend toward the higher score in the children with ADHD-HI and ADHD-C subtypes. It suggests that patients with the ADHD-I subtype tend to be hyporesponsive, whereas those with ADHD-HI and ADHD-C subtypes tend to be hyperresponsive. Corresponding to this, the proportion of participants whose score in any of the subsections of SP-2 was much less than others (<3^rd centile) was numerically more in the ADHD-I group and the proportion of participants whose score in any of the subsections of SP-2 was much more than majority others (>97^th centile) was numerically more in ADHD-I group. However, this difference was not statistically significant, suggesting the majority of ADHD patients had SP-2 subsection scores between the 3^rd and 97^th centile (i.e., “either less than others,” “just like the majority of others” or “more than the majority of others”). The difference between ADHD subtypes was numerically more discriminative for auditory processing scores; still, the difference was not statistically significant.

There was a moderate negative correlation between hyperactivity/impulsivity T-score and auditory processing scores in SP-2 (P < 0.05, r = −0.43). It suggests that ADHD patients with more hyperactivity/impulsivity have more auditory processing problems. There was a weak negative correlation between visual processing score and hyperactivity/ impulsivity T-score in CPRS-R, but a moderate negative correlation between visual processing score and learning problems T-score in CPRS-R. It suggests that probably due to underlying inattention or other inherent problems of ADHD, these patients suffer from learning issues, which could be related to slow and imperfect processing of visual stimuli. For vestibular processing, touch processing, and oral processing, no significant correlation was observed with the severity of ADHD symptoms in CPRS-R [Table 3]. It suggests although all sections of SP-2 are more significantly affected as compared to healthy controls, auditory and visual processing are more affected.

However, for the patients with ADHD-C type, there was a trend toward higher scores for vestibular processing, as compared to their counterparts, but it did not reach the point of statistical significance (P = 0.09). It suggests that, at least, a subset of ADHD patients have problems with balance and coordination. The inattention-related T-score in CPRS-R had a weak negative correlation with vestibular processing, suggesting inattention problems might be related to poor processing of balance and coordination-related issues in ADHD children. The forward digit span score and Corsi block span test score showed a moderate negative correlation with auditory and visual processing scores (r = −0.4–−0.6, reaffirming the previous findings. Both these findings suggest that inattention in ADHD patients might be related to poor auditory and visual processing or it might be because inattention in these children leads to poor auditory and visual processing.

There was a weak yet significant positive correlation between the severity of CD-related problems in CDRS-P, oppositional defiant problems in ODDRS, and anxiety problems in Screen for Child Anxiety-Related Disorders and auditory as well as tactile processing scores in SP-2 (P < 0.05, r−0.2–0.4). It suggests that ADHD patients with anxiety and more severe conduct/oppositional defiant problems tend to be hyperresponsive to sensory stimuli. The emotional-social response section score in the SP-2 score had a moderate positive correlation with anxiety and depression severity (r = 0.47 and 0.52, respectively). The executive function measured by BRIEF was lower as compared to healthy controls. However, apart from a weak positive correlation between the Global executive composite T-score and the auditory processing score (P < 0.05, r = 0.31), no other significant correlation was observed for other sections. In the quadrant score summary, the scores for all four types, that is, low registration, sensory sensitivity, sensation seeking, and sensation avoiding were significantly higher in the ADHD group as compared to healthy controls. However, the number of patients who had scored “much more than others” was higher for “low registration” and “sensory sensitivity” patterns compared to healthy controls and not for the other two patterns. Finally, we could not detect any significant difference between various section scores of SP-2 between patients receiving different medications. Moreover, there was no significant impact of other demographic variables such as age, gender, and SES on SP-2 scores suggesting that the abnormalities noted in ADHD patients were inherent to the disease characteristics.

DISCUSSION

Our study explores sensory processing problems in an Indian cohort of ADHD and compared them with healthy, typically developing controls. Consistent with previous clinical studies, our study also showed that ADHD children have more sensory processing abnormalities. However, unlike autistic children, who had often sensory symptoms evident from history and SP scores largely outside the reference range, children and adolescents with ADHD have more subclinical sensory problems, detectable only by performing detailed, objective evaluation.^[21] However, these sensory processing problems differ in extent and characteristics between ADHD subtypes. There was also a significant correlation between the severity of ADHD symptoms in some domains and the severity of some comorbid symptoms with sensory-processing abnormalities.

The finding in our study that sensory processing scores in most of the domains of SP-2 are different from the healthy controls has been shown in the study by Shimizu et al. from Brazil.^[13] Dunn and Bennett.^[22] also had similar findings and our cohort of ADHD patients resembles more to this cohort because the majority of children in this cohort were also receiving various medications like our cohort. Yochman et al.^[9] also found a significant difference for 11 out of 14 sections, except for vestibular processing, emotional response, and tone/endurance. However, they mainly included pre-schoolers. ADHD and sensory processing problems often change with the increase in age and probably the reason behind some disparities between the results of this study and our study.

Although most studies concluded about the existence of sensory processing problems in ADHD children, its type, severity, and clinical correlation with symptom profile varied across studies. While most studies showed some problems in visual and auditory processing problems, few studies had previously assessed tactile, vestibular, and olfactory processing abilities. While the majority of studies showed sensory hyper-responsivity to various modalities, some studies also demonstrated sensory hyporesponsivity. However, not all ADHD patients follow the same pattern of sensory abnormalities. Even different children with autism show different types of sensory abnormalities. For this purpose, in our study, we also tried to find out how many children showed scores in individual sections beyond the 97^th or 3^rd centile (much more or much less than the majority of others). However, a previous systematic review in this regard by Ghanizadeh.^[5] showed that ADHD patients with sensory hyper-responsivity showed more features of anxiety and oppositional defiant behavior. These findings have also been shown in our study, although the strength of the correlation was weak.

Parush et al.^[23] have previously shown that tactile defensiveness or hyperresponsiveness to tactile stimuli was more common in females. Our study probably did not reach such a conclusion, as we had only a few female participants in our study or it might be due to ethnic differences between the sample population of both studies.

At least one-third of children with ADHD have been shown to have significant problems in balance, coordination, and equilibrium in a study by Sergeant et al.,^[24] and they were found to suffer from developmental coordination disorder. Although few other studies have also shown problems with balance and coordination in children with ADHD, such high prevalence has not been shown in subsequent studies or our study.

Children with ADHD have been shown to have difficulty with auditory discrimination, auditory localization, both hyporesponsivity (under-registration of sound) and hyper-responsivity to sound.^[5] While ADHD-I type patients showed auditory hyporesponsivity, the opposite was true for the ADHD-HI type. The same trend was also observed in our study, although it missed the level of statistical significance, probably due to the small number of patients in the ADHD-I subgroup. Ghanizadeh.^[5] also have previously shown that patients with ADHD and co-occurring ODD are more likely to be hyporesponsive to auditory stimuli.

Stimulants have been suspected to induce visual hyperresponsivity or photophobia in a previous study by Ghanizadeh.^[5] However, this finding is not substantiated in our study, although formal visual field assessment was not part of our study. Future studies need to objectively evaluate various types of vision abnormalities before and after the use of stimulants.

Although abnormalities in sensory processing in ADHD subjects are less substantial than in autistic children and none of these patterns of abnormalities described are highly specific to be used as a discriminatory or diagnostic modality, it probably has some therapeutic implications. At least, those subjects having SP-2 scores fairly out of the normal range should be advised appropriate sensory integration therapy. Certain psychiatric comorbidities are more common in patients with sensory hyperresponsivity and need to be addressed appropriately. Almost all studies on ADHD patients in this regard are cross-sectional studies and have not explored the therapeutic implications. Miller et al. have shown that even occupational therapy can help patients with sensory modulation disorder. Whether the same holds true for ADHD patients or not needs to be evaluated. Pharmacotherapy in ADHD and other disorders has been proposed to modulate and sometimes even alleviate sensory issues. The existing literature, however, did not show any definite advantage or disadvantage of stimulants or other medications on sensory issues in ADHD patients.

The parent report version of SP-2 is only a subjective measure and might have underestimated or overestimated the sensory issues. Almost all previous studies have also focused on parent-report questionnaires. Future studies exploring more objective measures and laboratory tests like evoked potentials are likely to provide a more accurate description of sensory issues in ADHD patients. Anokhin et al.^[25] have proposed the possibility of putative genetic factors in the subclinical differences in evoked potentials in these patients. As these evoked responses are suspected to be somewhat different in ADHD patients as compared to the normal population, genetic polymorphism or mutation analysis in ADHD patients with significant sensory issues may provide yet unknown details of underlying genetic biomechanics.

Overall, our study is the first from the Indian subcontinent, which has systematically compared sensory issues in ADHD children and adolescents with healthy children and reaffirmed the findings in previous studies from other parts of the world. Due to several methodological limitations and heterogeneity of findings of various studies, it is difficult to reach a certain conclusion about a particular sensory abnormality pattern in ADHD patients.

CONCLUSION

Sensory processing abilities in ADHD children differ from that of typically developing children when objectively assessed, although most of the ADHD children had scores in the clinically normal range. The sensory processing profile also has an association with the severity and comorbidity profile of ADHD patients.