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A Literature Review of Gustatory Over-Responsivity Among the Population with Autism Spectrum Disorders

By Hyelee Kim, MD, MAS; Meelim Kim, PhD; Nahyun Kim, MD; Hosanna Kim, MD;Jae-Won Kim, MD, PhD; Elysa Marco, MD; Young Shin Kim, MD, MS, MPH, PhD

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Kim H, Kim M, Kim N, Kim H, Kim J, Marco E, Kim Y. A literature review of gustatory over-responsivity among the population with Autism Spectrum Disorders. HPHR. 2021;41.

A Literature Review of Gustatory Over-Responsivity Among the Population with Autism Spectrum Disorders

Abstract

Introduction

Atypical response to sensory stimuli is common in the autism spectrum disorder (ASD) population. While sensory over-responsivity in the gustatory domain (GOR) among ASD has been frequently reported, previous reviews were not solely focused on GOR in the ASD population. This review sheds light on pertinent sensory functions in ASD, differences in GOR between those with and without ASD, and concepts related to GOR in ASD.

Results

Neurobiological mechanisms in GOR were less studied in the population with ASD. Also, it is not clear if GOR is from difficulties of differentiation, detection threshold, and multisensory integration. Among thirty-six studies using behavioral questionnaires, a greater proportion of ASD (36-72%) had GOR compared to typically developing (TD, 20%) individuals. Furthermore, the ASD population repeatedly showed severe GOR scores relative to the TD cohort. Brain imaging studies suggested aberrant neural responses to oral stimuli as a contributing factor. It is posited that GOR contributes to food selectivity and poor dental care among ASDs. Poor nutritional outcomes among ASDs are controversial. However, severe GOR and food selectivity in reported cases present life-threatening events like pulmonary hypertension mediated by vitamin deficiencies. In addition, being underweight or overweight was associated with GOR in youths with ASD, raising a chronic health concern for general health and well-being. Another emerging consideration is the role of gut microbiome disruption in individuals with ASD and its relationship with GOR. Finally, the ASD population showed more common gastrointestinal problems than their TD counterparts, implying that GOR could be a consequence of anxiety from prior gastrointestinal experiences.

Conclusion

To provide families with ASD with an environment that promotes healthy development and growth, we need further research, development of clinical management, and policy changes. Thus, we recommend the targeted study of the neural mechanisms, microbiome consequences, and evidence-based intervention for GOR in ASDs.

Introduction

Sensory responsivity refers to how an individual modulates the environmental sensory stimuli and reacts to them.1,2 Sensory modulation disorder, one dimension of sensory processing disorders (SPD) included in the diagnostic classification of mental health and developmental disorders of infancy and early childhood, consists of sensory over-responsivity (SOR), sensory under-responsivity (SUR), and sensory craving (SC).2,3 SOR entails exaggerated and prolonged negative behavioral responses and avoidance of typically non-noxious stimuli, and the terminologies of SOR and hyper-reactivity/sensitivity have been interchangeably used.2 The prevalence of SOR varied according to the cut-off scores, diagnostic measures, and sensory domains applied in the studies. Based on parent report measures, 5-21% of children have SOR.4,5 SOR is more prevalent in populations with developmental disorders or mental health conditions such as ASD and attention-deficit hyperactivity disorder (ADHD), including those with autism spectrum disorder (ASD) and ADHD, and is closely related to social and emotional problems of children.6–8 Particularly, for the diagnosis of ASD, a neurodevelopmental disorder characterized by deficits in social interactions and communication and presence of repetitive and restricted behaviors, abnormal sensory reactivities are included in DSM-5 diagnostic criteria.9–11 A genetic study of 12,419 Swedish twin pairs aged 9 to 12 years found that SOR and ASD traits were highly inheritable and genetically correlated.12 A meta-analysis of 55 questionnaire studies of 4,606 individuals with ASD revealed that SOR was the only consistent factor that distinguishes an ASD group from developmental disorders (DDs) groups  suggesting that SOR is a significant feature of ASD.10 SOR contributes to emotional and social dysfunction and maladaptive behaviors in ASD, contributing to family impairments and distress.13–17

 

Oral stimuli, usually generated from food and occasionally from non-food-related actions such as teeth brushing, could be defined by different sensations in taste, texture, smell, and temperatures felt inside and around the oral cavity. Gustatory over-responsivity (GOR) could be expressed as avoidance, hypersensitivity, and aversive response to those sensory stimuli. The ASD population has shown a unique reactivity to gustatory stimuli.18–21 In a narrative interview of a focus group with six adults with ASD, individuals with ASD could not adapt to the smell, textures, or mixtures of foods and took more time than those without ASD to get used to such stimuli.22 Individuals with ASD also showed more maladaptive feeding and eating behaviors than typically developing (TD) counterparts, thereby contributing to psychological distress for parents.23,24 Moreover, these properties could hinder the appropriate development of children and cause acute and chronic health outcomes, such as nutritional deficiencies and their consequences as well as being overweight/underweight.25–28 Therefore, it would be essential to understand the characteristics of GOR and its trajectories to provide appropriate clinical care in the ASD population and mitigate future adverse health outcomes.

Previous reviews on gustatory and its related domains in ASD focused on sensory functions such as discrimination and detection abilities of tastes rather than behavioral response aspects.29–31 Also, prior literature reviews on food selectivity in ASD focused on nutrient intake or addressed the broad concept of SOR rather than GOR.32–34 To address these gaps, we aim to review sensory over-responsiveness/hyperreactivity in the gustatory domain, namely GOR, in the population with ASD. We intend to provide insights on the relationship between GOR and sensory functions, comparison of GOR in individuals with and without ASD, and its relationship with food selectivity, oral care, gastrointestinal (GI) problems, and microbiomes in the ASD population.

SOR is more prevalent in populations with developmental disorders or
mental health conditions such as ASD and attention-deficit hyperactivity
disorder (ADHD), including those with autism spectrum disorder (ASD)
and ADHD

Methods

     In this narrative review, we identified studies using terms related to GOR, such as “gustatory,” “taste,” “food selectivity,” “eating,” “feeding,” “diet,” “sensory processing,” “over-responsivity,” “reactivity,” and “sensitivity” and ASD, such as “ASD,” “autism,” “autistic,” “pervasive,” and “Asperger” in Pubmed, Embase, PsycInfo, and Google Scholar from 1990 to 2020. We also identified studies related to gustatory and olfactory functions, possible outcomes of GOR, its relationship with GI symptoms and microbiomes in the ASD population. We included published literature written in English regardless of participant age.

Results

Relationship of GOR with gustatory and olfactory sensory functions in ASD

Currently, limited studies address whether GOR results from enhanced discrimination and detection abilities in sensory domains or challenges in multisensory integration in the ASD population. Moreover, various measures were adopted, making it challenging to integrate study results.29 Neurobiological mechanisms in GOR were less studied in clinical research on ASD.29,35–37

 

A genetic variant in the taste receptor responsible for bitter sensitivity led to GOR in children with ASD.38 In a case-control study among 48 children with and without ASD, the ASD group showed lesser accuracy in identifying sour and bitter tastants than TDs.39 Adults with ASD did not show differences in threshold and hedonic responses to sweet tastes compared with healthy controls; however, ASD severity was associated with sweet sensitivity.40 In a study focusing on discrimination ability, adults with ASD showed low performance in identifying tastes and usually misidentified tastes as salty or no taste.41

 

Prior studies about olfactory sensory functions among the ASD population were not consistent but suggested that these functions could differ according to age, sex, and disease severity.31,29,42–44 One study pursued the association between olfactory function and brain activity in ASD using magnetic resonance imaging.45 In this case-control study (n=36), adults with ASD showed decreased olfactory function coupled with reduced activation of the piriform cortex compared to TDs.

Comparison of GOR in populations with and without ASD in previous studies

Comparison of GOR among those with and without ASD was conducted mainly using behavioral questionnaires and neuroimaging studies. Among 15 studies conducted using the Sensory Profile (SP), one of the widely used questionnaires, individuals with ASD showed greater GOR estimated by the oral sensitivity score. Preschool and elementary school-aged children with ASD had significantly more severe oral sensitivity scores than TDs (p<0.001).46 The proportion of GOR among the ASD group varied from 36% to 64%, whereas TD was 3-7%.46,47 In a cross-sectional study, the ASD group showed both GOR and gustatory sensory craving symptoms compared with the TD group.48 In this study, those abnormal sensory symptoms were more significant in the young ASD group than in the older ASD group. Among studies using the Short Sensory Profile (SSP), the shorter version of the SP, the taste/smell sensitivity score differed between ASD and TD groups. It also differed between ASD and developmental disability groups.49 In children with ASD, the prevalence of GOR estimated using the SSP varied from 41% to 72%, whereas 80-98%  of TDs did not show atypical responses.46,50–53 Similar results were repeated using different behavioral measures (Table1).54–57 In Woodard et al., toddlers (n=16) with and without ASD and demonstrated different heart rate responses after seeing food items among ASDs compared to TDs.58 Confronted to the oral stimuli, a higher proportion of the ASD group showed increased HR compared to the baseline than TD group, indicating physiological hypersensitivities.

 

 Table 1. Results of behavioral measures on gustatory over-responsivity among individuals with autism spectrum disorder

Study

(Year)

Population

Sex

M:F

Age

Range,

mean (SD)

Cognitive ability

Range, mean (SD)

Measure

Findings

Mean (SD)

Ermer and Dunn (1998)

Autism or PDD (n=38)

ADHD (n=61)

TD (n=1,075)

 

Autism or PDD 3-13 yrs

ADHD 3-15 yrs

TD 3-10 yrs

 

Sensory Profile

The oral sensitivity factor score showed a good discrimination ability for ASD from both ADHD and TD.

Talay-Ongan et al. (2000)

Autism (n=30)

TD (n=30)

27:3

4-14 yrs

 

Sensory Sensitivity Questionnaire-Revised

Gustatory modality scores

ASD 3.40 (0.79) and TD 1.40 (0.72) (p<.0001)

Watling, Deitz, and White (2001)

Autism (n=40)

TD (n=40)

7:1

3-6 yrs

 

Sensory Profile§

Oral sensitivity factor scores

ASD 26.3 (8.6) vs. TD 36.1 (6.9) (p<.0001)

Dunn et al. (2002)

Asperger syndrome (n=42)

TD (n=42)

39:3

8-14 yrs

 

Sensory Profile§

Oral sensory processing section score (12 items)

Effect size (η2): 0.39 (p<.001) (large effect size)

ASD 42.7 (1.5) vs. TD 54.9 (1.2)

Oral sensitivity factor score (9 items)

Effect size (η2): 0.29 (p<.001) (large effect size)

ASD 30.8 (1.3) vs. TD 40.0 (1.0)

Rogers, Hepburn, and Webner (2003)

Autism (n=26)

Fragile X syndrome (n=20)

DD of mixed etiology (n=32)

TD (n=24))

 

Autism 26-41 mos

Fragile X syndrome 21-50 mos

DD 24-47 mos

TD 12-35 mos

 

Short Sensory Profile§

The autism group showed more abnormal responses to taste and smell than all other groups.

Taste/smell sensitivity section score

Autism 11.09 (4.8) vs. TD 17.58 (2.5) (p<.0001)

 

Adamson et al. (2006)

ASD (n=44)

37:7

115.2 (38.0) mos

 

Short Sensory Profile

Definite difference taste/smell section score: 41%

Probable difference taste/smell section score: 11%

Kern et al. (2006)

Autism (n=104)

Community controls (n=104)

79:25

3-56 yrs

 

Sensory Profile

Oral sensory processing dysfunction:

Autism > control (p<.0001)

Low threshold symptoms (GOR):

Autism > control (p<.0001)

GOR decreased as an individual with autism became older.

Baranek et al. (2006)

Autism (n=56)

PDD (n=24)

DD/ID (n=33)

Other DD (n=35)

TD (n=110)

 

Autism 23-80, 40.47 (12.76) mos

PDD 26-73, 39.14 (10.81) mos

DD/ID 11-56, 33.72 (9.17) mos

Other DD 16-64, 33.40 (10.86) mos

TD 5-49, 29.30 (11.55) mos

 

Sensory Experience Questionnaire

1 item related to GOR (avoids food taste/texture)

ASD 3.91 (1.23) vs. PDD 3.29 (1.52) vs. DD Combined 2.60 (1.39) vs. TD 2.54 (1.25)

Tomchek and Dunn (2007)

ASD (n=281)

TD (n=281)

ASD 211:45

TD 235:43

3-6 yrs

 

Short Sensory Profile

Definite difference taste/smell section score (2 SD)

ASD 54% > TD 7%

Leekam et al.

Study 1

(2007)

Low functioning autism (n=16)

High functioning autism (n=17)

DD (n=19)

Language impairment (n=15)

TD (n=15)

Low functioning autism 15:1

High functioning autism 14:3

DD 11:8

Language impairment 10:5

TD 9:6

Autism 33-134 mos

DD 40-140 mos

Language impairment 33-138 mos

TD 51-135 mos

High functioning autism and language impairment non-verbal IQ >80

Low functioning autism and DD non-verbal IQ <80

TD IQ 81-138

Diagnostic Interview for Social and Communication Disorders

Proportions of severe score ranges in smell/taste items

ASD 31-47% > TD 0-7%

Leekam et al.

Study 2

(2007)

Autism (n=200)

 

32 mos-38 yrs

High functioning group IQ>70

Low functioning group IQ<70

Diagnostic Interview for Social and Communication Disorders

Proportions of severe smell/taste scores

51-57% of the low functioning group

46% in younger and 26% in older

37-43% of the high functioning group

32% in younger and 12% in older

Brown et al. (2008)

ASD (n=26)

TD (n=26)

ASD 21:5

TD 18:6

5-8 yrs

 

Sensory Profile§

Oral sensory processing section score

Effect size (partial η2): 0.42 (large effect size)

ASD 37.39 (9.68) vs. TD (52.39 (7.35) (p<.01)

Oral sensory sensitivity factor score

Effect size (partial η2): 0.34 (large effect size)

ASD 27.69 (9.01) vs. TD 39.04 (6.38) (p<.01)

Jou et al. (2009)

Autism (n=22)

TD (n=22)

22:0

Autism 8.1-13.9 yrs

TD 7.9-13.0 yrs

ASD IQ 64-128, 92.3 (17.0)

TD IQ 91-134, 116.9 (13.1)

 

Sensory Profile§

Oral sensory sensitivity factor score

ASD 27.1 (9.1) vs. TD 44.1 (2.5) (p<.001)

Corbett et al. (2009)

Autism (n=22)

TD (n=22)

Autism 21:1

TD 19:3

6-12 yrs

Autism IQ 87.9 (11.9)

TD IQ 113.6 (15.5)

Short Sensory Profile§

Taste/smell sensitivity section score

Autism 9.0 (4.2) vs. TD 18.4 (2.6)

Schoen et al. (2009)

ASD (n=38)

Asperger syndrome (n=11)

High functioning autism (n=27)

SMD (n=31)

TD (n=31)

 

Autism 5-15 yrs

SMD 5-13 yrs

TD 4-12 yrs

 

Short Sensory Profile

Definite difference taste/smell section score (2 SD)

ASD 61% vs. SMD 42%

Taste/smell sensitivity section scores

Severest: ASD > SMD > TD

ASD vs. TD (p<.001)

SMD vs. TD (p<.001)

ASD vs. SMD (p=.056)

O’Brien et al. (2009)

Autism (n=34)

LD (n=22)

TD (n=33)

 

Autism 9.8 (4.5) yrs

LD 9.3 (5.0) yrs

TD 9.7 (5.3) yrs

 

Adapted Short Sensory Profile§

Taste/smell sensitivity section scores

Autism 10.28 (5.5) vs. TD 17.24 (3.84) (p<.01)

Cheung and Siu (2009)

ASD (n=72)

ADHD (n=114)

TD (n=1,840)

TD 925:915

ASD 2.7-11.6 yrs (5.4 (5.4))

ADHD 4.8-12 yrs (7.9 (1.4))

TD 3-10 yrs (7.25 (2.8))

 

Chinese Sensory Profile

In the overall comparison, the taste/smell subscale differed in groups of ASD, ADHD, and TD (p<.001).

All items in the subscale differed between ASD and TD groups (p<.001).

Wiggins et al. (2009)

ASD (n=17)

DD (n=17)

27:7

17-45 mos

 

Short Sensory Profile

Taste/smell sensitivity section score

ASD 11.6 (5.3) vs. DD 16.0 (4.0) (p=.01)

Hilton et al. (2010)

High functioning ASD (n=36)

TD (n=26)

ASD 31:5

TD 22:4

6-10 yrs

ASD IQ 102.2

TD IQ 106.5

Sensory Profile§

Oral sensory processing section score

High functioning ASD 22.74 vs. TD 43.63 (p<.01)

Hochhauser & Engel-Yeger (2010)

High functioning ASD (n=25)

TD (n=25)

ASD 17:8

TD 18:7

ASD 8.41 (1.44) yrs

TD 8.41 (1.47) yrs

IQ >70

Short Sensory Profile§

Taste/smell sensitivity section scores

ASD vs. TD: 9.08 (2.67) vs. 17.36 (2.39) (p<.0001)

Nadon et al. (2011)

ASD (n=95)

87:8

3-10 yrs

 

Short Sensory Profile

The total SSP score was associated with the number of eating problems after adjusting age, mental retardation, and comorbid ADHD.

Woodard et al. (2012)

ASD (n=8)

TD (n=8)

7:1

2-3 yrs

 

6 food items challenge

Food items: dry cereal, wet cereal, cold chicken, warm chicken, sour candy, sweet sucker

Among 48 available heart rate observations after food challenges

ASD HR ↑ 12 vs. HR ↓ 1

TD HR ↑ 10 vs. HR ↓ 10

 

Brockevelt et al. (2013)

Autism (n=21)

TD (n=21)

 

3-9 yrs

IQ>50

Sensory Profile§

Oral sensitivity factor scores

Autism 28.24 (5.01) vs. TD 40.95 (9.50) (p<.001)

Tavassoli et al. (2014)

ASD (n=221)

TD (n=181)

ASD 115:106

TD 129:52

ASD 38.7 (12.0) yrs

TD 37.2 (12.9) yrs

 

Sensory Processing Scale

While both smell and taste section scores differed significantly between groups (p=.0001), SOR correlated positively with autistic traits.

Kral et al. (2014)

ASD (n=25)

TD (n=30)

ASD 18:7

TD 14:16

4-6 yrs

 

Sensory Profile§

Oral sensory sensitivity score

ASD 29.4 (10.4) vs. TD groups 39.5 (8.5) (p<.001)

Definite difference range oral sensitivity score

ASD 44% vs. TD 7%

Tanner et al. (2015)

ASD with food selectivity (n=17)

ASD without food selectivity (n=18)

ASD with food selectivity 15:2

ASD without food selectivity 17:1

Food selectivity group

79 (22.5) mos

Non- selective group

83.6 (23.4) mos

 

Short Sensory Profile

Both groups showed atypical taste/smell sensitivity section scores

Food selectivity ASD 9.17 (4.60) vs. Non-selective 12.28 (4.38)

The taste/smell sensitivity score was correlated with total foods eaten, limitation of variety, and food refusal.

Kuschner et al. (2015)

High-functioning ASD (n=65)

TD (n=59)

High-functioning ASD 58:7

TD 54:5

ASD 16.3 (3.1) yrs

TD 17.3 (2.8) yrs

ASD verbal IQ 109.8 (17.0), performance IQ 108.0 (14.3), full IQ 110.4 (15.5)

TD verbal IQ 112.6 (12.3), performance IQ 112.6 (11.2), full scale IQ 114.4 (10.9)

Adolescent/Adult Sensory Profile

ASD group reported greater food neophobia and disliking foods with particular textures and strong tastes (for all, p<.005). After adjusting the global sensory sensitivity, differences for disliking textured foods and strong tastes remained statistically significant between ASD and TD groups.

Al-heizan et al. (2015)

ASD (n=46)

TD (n=30)

ASD 7:39

TD 6:24

ASD 3-10 years (6.50 (2.40))

TD 2-10 years (6.40 (2.14))

 

Short Sensory Profile

Definite difference and probable difference taste/smell sensitivity scores

ASD 52% and 20% vs. TD 3% and 17%

Taste/smell sensitivity scores

ASD 11.7 (5.0) vs. TD 16.6 (2.5)

McCormick et al. (2016)

ASD (n=29)

DD of mixed/unknown etiology (n=26)

TD (n=24)

 

ASD 26-41 mos (33.75 (3.7))

DD 24-47 mos (33.40 (6.7))

TD 12-35 mos (19.57 (4.7))

 

Short Sensory Profile

Parents in the ASD group reported more taste sensory symptoms than parents in the DD group.

More severe taste/smell sensitivity in ASD than in both DD and TD groups.

Shmaya et al. (2017)

ASD (n=50)

Sibling (n=12)

TD (n=29)

ASD 41:9

Sibling 10:2

TD 22:7

ASD 54 (11) mos

Sibling 77 (32) mos

TD 52 (12) mos

 

Sensory Profile

In the ASD group, the oral sensory sensitivity factor (GOR), as well as other sensory processing dysfunctions, were significantly related to food selectivity (p<.05).

Chistol et al. (2018)

ASD (n=53)

TD (n=58)

ASD 83:17

TD 78:22

3-11 yrs

 

Sensory Profile

Taste/smell sensitivity score in probable (1 SD-2 SD) and definite (2 SD) difference scores¶

ASD 10% and 56% vs. TD 7% and 2%

Oral sensory sensitivity factor scores in probable and definite difference

ASD 28% and 36% vs. TD 3% and 3%

Oral sensory sensitivity factor scores

ASD 29.6 (8.4) vs. TD 40.6 (5.2) (p<.001)

Within the ASD group, children with GOR showed more food refusal (p<.001), limited vegetable variety (p<.001), food repertoire (p=.08), and fruit variety (p=.003).

Little et al. (2018)

ASD (n=77)

ADHD (n=78)

TD (n=84)

ASD 63:14

ADHD 61:17

TD 63:21

3-14 yrs

 

Child Sensory Profile 2

While there was some overlap of sensory processing patterns in ASD and ADHD, the ASD group showed the severest score in oral sensory processing (p<.001).

Avery at al. (2018)

ASD (n=21)

TD (n=21)

21:0

ASD 21 (3) yrs

TD 22 (3) yrs

ASD 110.9 (13.8)

TD 119.52 (9.93)

Adolescent/ Adult Sensory Profile

Adapted taste reactivity

ASD 11 (4) vs. TD 8 (3) (p<.01)

 

Kojovic et al. (2019)

ASD (n=64)

TD (n=36)

ASD 55:9

TD 26:10

3-6 yrs

ASD 78.3 (26.2)

TD 113 (13.4)

Short Sensory Profile

The taste/smell sensitivity score was more severe in the ASD group compared to the TD (p<.001).

Jussila et al. (2020)

ASD (n=28)

Non-ASD (n=4369)

ASD 17:11

Non-ASD

2150:2219

8 yrs

IQ>50

14 item parental questionnaire

ASD group was 7.98 times more likely to have GOR than the non-ASD group (RR 7.98 (95% CI: 1.96-32.53, p=.0007) (transformed from OR based on table2).

In the non-ASD group, GOR was associated with an autistic trait score.

GOR+ 8.2 (9.5) vs. GOR- 3.3 (5.3) (p<.001)

In the ASD group, autistic trait scores did not differ according to GOR.

GOR+ 41 (11.3) vs. GOR- 42.6 (10.7) (p=.74)

Viviers et al. (2020)

ASD (n=21)

TD (n=21)

ASD 16:5

TD 10:11

3-5 yrs

 

Brief Autism Mealtime Behavioral Inventory

While the ASD group showed more food selectivity and atypical mealtime behaviors, they also showed statistically significant, more severe scores in the broad concept of sensory processing in the gustatory domain.

Note: ADHD=attention deficit hyperactivity disorder, ASD=autism spectrum disorder, DD=developmental disability, GOR=gustatory over-responsivity, HR=heart rate, IQ=intelligent quotient score, LD=learning disability, OR=odds ratio, PDD=pervasive developmental disorder, SD=standard deviations, SMD= sensory modulation disorder, TD=typically developing, yrs=years, mos=months,

  • Lower scores mean more severity in the Sensory Profile and the Short Sensory Profile.

¶ In this article, the authors defined taste/smell section items in the SSP and referred to it as oral sensory over-sensitivity

Limited neuroimaging studies have been published on GOR among individuals with ASD (Table 2). Jou et al. found that brainstem gray-matter volume showed a positive association with oral sensitivity score, suggesting that the reduction in brainstem gray-matter might be related to GOR in ASD.59 Another neuroimaging study showed higher hemodynamic activity in the bilateral insula and anterior cingulate cortex among adolescents with ASDs to palatable food pictures than in the TDs, indicating aberrant neural responses to primary rewards.60 In addition, adults with ASD showed an association between GOR score and brain responses related to gustatory perception and rewards when actual sweet tastants and food pictures were used.61

Table 2. Results of imaging studies on gustatory over-responsivity (GOR) among individuals with autism spectrum disorder

Study

(year)

Population

Sex M:F

Age (yrs)

mean (SD)

Cognitive ability

range, mean (SD)

Measures

Findings

Jou et al. (2009)

Autism (n=22)

TD (n=22)

22:0

Autism 8.1-13.9

TD 7.9-13.0

Autism IQ

(64-128, 92.3 (17.0))

TD IQ

(91-134, 116.9 (13.1))

 

Sensory Profile, MRI

A significant association between brainstem gray-matter volume and oral sensory sensitivity in ASD group (r=0.38, p<.01).

Cascio et al. (2012)

ASD (n=17)

TD (n=18)

ASD 17:0

TD 17:1

ASD

12.8 (2.5)

TD 13.2 (3.4)

ASD IQ

111.56 (12.99)

TD IQ

103.72 (13.22)

fMRI

Hemodynamic reactivity to pictures of palatable foods in adolescents with ASD was greater in the insular and anterior cingulate cortex.

Both groups showed responses in the amygdala, nucleus accumbens, insula, and orbitofrontal cortex.

Avery et al. (2018)

ASD (n=21)

TD (n=21)

21:0

ASD 21 (3)

TD 22 (3)

ASD

110.9 (13.8)

TD

119.52 (9.93)

Adolescent/ Adult Sensory Profile, fMRI

The self-reported GOR in ASD was associated with heightened brain responses to food-related stimuli and atypical functional connectivity of the primary gustatory cortex.

Note: ASD=autism spectrum disorder, GOR=gustatory over-responsivity, (f)MRI= (functional) magnetic resonance imaging, SD=standard deviations, TD=typically developing, yrs=years

Impacts of GOR in ASD population: food selectivity, challenges in dental care, and nutritional outcomes

Food selectivity among ASD is common, especially persisting longer periods in life.24,46,62–64 Trajectory studies reported subgroups among ASD in which severe feeding problems continued to persist during adulthood.65,66 Furthermore, it is closely related to problematic mealtime behaviors, which causes more familial distress to the ASD population.24,32,67–69 Food selectivity persisted even when adaptive functioning was adjusted: within the same level of adaptive functions, 67% of the ASD group continued to have problematic feeding and eating behaviors as opposed to 33% of the TD.68

 

GOR to texture, smell, tastes, colors, and mixtures of foods could contribute to food selectivity in the ASD population.18,21,46,70,71 Among ASD children, GOR and other sensory modulation dysfunctions were associated with food selectivity.72 GOR was still associated with eating problems after adjusting the age, intellectual disability, and comorbid ADHD.21 ASD children with GOR were reluctant to try novel foods, refused to eat certain kinds of foods, consumed limited types of foods, and were more likely to eat less owing to negative emotions.46,47,73,74 Youth with ASD reported that they disliked certain textures and strong tastes, and more children with ASD pointed out textures and flavors as the reason for refusal.20,75,76 Textures were the most common factor for GOR in ASD, whereas the colors of foods also accounted for GOR.77 That is, individuals with ASD and SOR occasionally prefer white or colorless foods, which might decrease the sensory overload.77 Sex-difference in GOR might exist. Females with ASD endorsed more eating problems and GOR than males.78 Researchers also pointed out that the motor impairments per se could cause aversive responses to gustatory stimuli. Children with ASD who more often refused foods had a greater prevalence of malocclusion of teeth and poorer periodontal health.79

 

Consequently, food selectivity among children with ASD may result in insufficient nutrient consumption. Studies investigating whether food selectivity among ASD individuals is related to the inadequate intake of specific nutrients remain controversial.32–34,80,81 Nonetheless, some cases have reported extreme deficiencies of nutrients, such as vitamin C, vitamin A, vitamin B3, and iron.82–86 These severe nutrient deficiencies like scurvy and pellagra are rare in developed countries, resulting in delayed diagnosis and severe outcomes, such as pulmonary hypertension and intracranial hypertension.34,82,84,87 In addition, insufficient intake of protein, calcium, and phosphorus is associated with lower bone mineral densities among ASDs.88 A trajectory study found that children with ASD had a limited repertoire of foods even with time passed and were prone to weight gain.89 Although the sample size was small (n=18), participants with ASD included in the obesity/overweight strata increased from 28% at baseline to 50% after six years of follow-up. While both underweight and overweight issues have been reported to be associated with GOR, the prevalence of obesity among children and adolescents with ASD is higher than TDs in developed countries like the U.S., deeming significant chronic health risks.90–93

 

Additionally, dental care problems among the ASD population have been reported.79,94–97 While children with ASD are exposed to high sugar content, about half were treated for dental care.96 Also, ASD children with SOR reported more difficulties in dental care at home and clinical settings than ASD children without SOR.97 A systematic review of 10 studies found a worse outcome in oral, gingival, and periodontal hygiene care among children with ASD younger than 18 years with ASD compared to TD counterparts.

GOR, GI problems, and microbiomes in the ASD population

So far, we discussed how GOR among ASDs could differ from TDs and possible consequences. However, questions about why individuals with ASD pursue only certain types of food while meticulously limiting others remain unclear.98 Recently, the relationship between GI problems, diet, and microbiomes among the ASD population has been investigated.98–102 Microbiome investigations have reported that gut colonization can affect the brain-gut–microbiome axis.103–105 Microbiomes could affect the development of ASD through synaptic pruning in the brain.106 Interestingly, gut and oral microbiomes in the ASD population were different from the healthy controls.100,107–109 Treatments that affected microbiomes were associated with the behavioral changes of ASD.110 We need microbiomes to digest foods and absorb nutrients.111 Given that the researchers argue that the variation in microbiomes among individuals with ASD could give rise to abdominal pain and discomfort to certain food types, leading to the avoidance and refusal of such foods.98,112 Mulle et al. suggested that reduced microbiomes responsible for vegetable digestion in ASDs might induce discomfort, thereby limiting food repertories that cannot be digested.98

 

Additionally, the prior experience of GI problems and uncomfortable feelings and memories could influence GOR in the ASD population. Functional and medical GI problems are common in ASD.113–116 Patients with ASD showed a higher prevalence of inflammatory bowel disease and other GI disorders and more severe GI index scores than their TD counterparts.117,118 Eosinophilic esophagitis was also found among children with ASD and feeding disorders.115,119 The ASD population and their relatives had greater intestinal permeability, associated with food allergies and hypersensitivities.120,121 Children with ASD showed higher past and current GI symptoms (vomiting, diarrhea, constipation, and abdominal pain) than TDs (47% vs. 22%).113 The authors also found that past incidences of vomiting and diarrhea and the existing constipation problem were significantly greater among the individuals with ASD than TD individuals. Compared with their siblings, the ASD group had more frequent GI problems of constipation and chronic diarrhea (42% vs. 12%, p<0.001).122 A meta-analysis of 15 studies revealed an increased odds ratio of 4.2 (95% CI: 1.90, 10.28) for general GI concerns.116 Among 2,973 ASD children, 25% had chronic GI problems; compared with those without GI problems, those with chronic GI problems had a more severe SOR score (64.6 vs. 70.9, p<0.0001).123 In this study, the number of GI problems increased as the child exhibited more SOR, and SOR scores had a statistically significant negative correlation with anxiety (p<0.0001). Of 225 children with ASD, 26% experienced chronic abdominal pain at baseline, and 87% of these children had persistent abdominal pain even after a year; however, 24% of the children without any symptom at baseline eventually developed abdominal pain.124 A study also showed an association between SOR, anxiety, and chronic abdominal pain among ASDs.125

Discussion and Implications

This review found that GOR estimates in the behavioral measures showed more severe scores in the ASD population than the TDs, with the majority of studies conducted in pediatric populations.55 Out of 36 studies conducted using behavioral measures, only four included adults, of which one study was exclusively an adult cohort.20,48,55,61 Moreover, many studies in this review were conducted on males, despite a recent study reporting that SOR is more common in females with ASD than males.126 Additionally, only 11 out of 36 behavioral studies reported the cognitive test results, and children outside of a certain cognitive range were excluded from those studies. Thus, it is difficult to deduce information about GOR among individuals with low cognitive abilities from the available data. Therefore, caution should be exercised while applying the study results to those populations. We also need studies conducted in a larger and more representative sample to apply our findings to subgroups within a broad ASD population.

 

In addition, while various sensory measures were developed, GOR estimates of behavioral measures are not specific to SOR but reflect any disruption in the gustatory or olfactory domains.56,127,128 Moreover, behavioral questionnaires could be a subjective tool. Variances and biases can arise depending on the measurer’s memory, cognition, and perception of GOR. Test-retest reliability and inter-rater reliability of the gustatory domain were reported in a few behavioral questionnaires.129,130 Given that, we need to interpret GOR estimates using behavioral questionnaires combined with other clinical measures and diet assessments, such as direct clinical behavioral assessments and food intake questionnaires.130–132

 

Although apparent differences in GOR have been consistently found between the ASD group and other populations, whether peripheral or central sensory neural abnormalities cause SOR remains unclear. GOR could arise from enhanced discrimination or detection ability of the gustatory or olfactory domains or enhanced or aberrant transmissions conducted via the higher neuro-cortical circuits.59–61 Additionally, differences in the microbiome or prior GI problems could provoke anxiety and over-response to even non-aversive gustatory sensory stimuli. While studies on microbiome opened a new area for understanding the mechanisms and possible interventions, many microbiome studies were small and cross-sectionally administered. Thus, we cannot differentiate the effect of unique microbiomes from confounding factors, including diet, birth delivery method, and antibiotic usage.99,133,134 Therefore, we need to perform a prospective longitudinal cohort study that enables us to administer the research question on the causal relationship of microbiome and GOR among ASD populations.  Finally, we need to educate and increase the awareness of the importance of GOR among students, trainees, and clinicians who work for the population with ASD. Also, we need to implement policies that could reduce adversities and distresses from GOR among families with ASD to provide children with ASD and their families with an environment that they can develop socially and emotionally appropriately. It would be required to develop and provide educational opportunities and interventions that target GOR for families with ASD in clinical settings.

Conclusion

Compared to other sensory abnormalities, GOR was less recognized in clinical and research settings. However, given the daily impact of GOR on patients and families with ASD, more clinical attention and rigorous systematic research on GOR in ASD are needed in the future. Additionally, the implementation of policies to fund population-based microbiome studies and evidence-based intervention to manage GOR in those with ASDs will be critical in improving the quality of life and prognosis of individuals with ASD.

Acknowledgements

We want to express our sincere thanks to Dr. Evans Whitaker, the research librarian at University California San Francisco (UCSF), and Dr. Isabel Elaine Allen, a professor of the department of biostatistics at UCSF, for providing valuable advice on designing our manuscript.

Disclosure Statement

All authors of this publication declare that they have no conflicts of interest.

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About the Author

Hyelee Kim, MD, MAS

Hyelee Kim, MD, MAS, is a board-certified psychiatrist in South Korea and a graduate student of the neuropsychiatric epidemiology program of the Harvard T.H. Chan School of Public Health. Her research interest is on increasing access to care for psychiatric disorders.

Meelim Kim, PhD

Meelim Kim, PhD, is a research assistant professor in the Health IT-Center at Yonsei University Health Systems and a postdoctoral scholar in the Center for Wireless and Population Health System at the University of California San Diego. Her research areas include digital behavioral interventions and precision medicine.

Nahyun Kim, MD

Nahyun Kim, MD, is a resident of the physical medicine and rehabilitation program of the Burke Rehabilitation Hospital in New York. She received her medical training at Seoul National University College of Medicine in South Korea and finished her preliminary training in internal medicine at Flushing Hospital Medical Center.

Hosanna Kim, MD

Hosanna Kim, MD, is a resident of the department of psychiatry and behavioral sciences at the University of California Davis and completed her postdoctoral training in the University California San Francisco Center for autism spectrum disorder and neurodevelopmental disorders.

Jae-Won Kim, MD, PhD

Jae-Won Kim, MD, PhD, is a professor in the department of psychiatry & behavioral sciences of the Seoul National University Hospital and the Seoul National University Children’s Hospital in South Korea.

Elysa Marco, MD

Elysa Marco, MD, is the professor in the department of pediatric neurology and the executive director of the neurodevelopmental medicine program at Cortica Healthcare. She is also a research associate at the University of California San Francisco.

Young Shin Kim, MD, MS, MPH, PhD

Young Shin Kim, MD, MS, MPH, PhD is the professor of the department of psychiatry and behavioral sciences at the Weill Institute for Neurosciences, University of California San Francisco, and the director of the center for autism spectrum disorder and neurodevelopmental disorders.

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