Factors Associated with Receptive and Expressive Language in Autistic Children and Siblings: A systematic review

doi:10.21203/rs.3.rs-1829194/v1

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Factors Associated with Receptive and Expressive Language in Autistic Children and Siblings: A systematic review

https://doi.org/10.21203/rs.3.rs-1829194/v1

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Background

Language abilities of autistic children and children at elevated likelihood for autism (EL-siblings) are highly heterogeneous, and many of them develop language deficits. It is as of yet unclear why language abilities of autistic children and EL-siblings vary, although a multifactorial risk model for language deficits seems more plausible than a single exploratory factor. In this review, we discuss research articles that identify factors implicated in the receptive or expressive language abilities of autistic children and EL-siblings since the introduction of the DSM-5.

Method

The search strategy of this review followed the PRISMA guidelines. The following databased were consulted: Embase, MEDLINE, Web of Science Core Collection and Scopus. Risk of bias (ROB) assessment was completed on using the Newcastle-Ottawa Scales.

Results

Out of 25624 records screened, 54 articles were included. We identified 56 factors implicated in receptive or expressive language abilities of autistic children and EL-siblings and divided them into ten categories: autism traits; biological factors; brain-based factors; child characteristics and early child development; environmental factors; gestures; motor skills; parental input; social factors and other factors. Although many of the identified variables were only examined in one article, some well-researched factors stood out, in particular joint attention, nonverbal cognitive abilities and frontal EEG power.

Conclusions

Our results confirm that a multifactorial risk model is most likely for language deficits in autism. Important aspects that should be considered in such a model are, amongst others, social factors such as joint attention, child characteristics such as nonverbal cognition, and neurocognitive factors.

autism

young children

language

systematic review

Language abilities are highly heterogeneous in children with autism spectrum disorder (henceforth autism) [e.g., 1, 2, 3], a neurodevelopmental condition characterized by challenges in social communication and social interaction, and restricted and repetitive behaviors [4]. Apart from the pragmatic aspect of language involved in social communication which is inherently difficult for autistic children [e.g., 5, 6, 7], some of these children also experience structural language difficulties [5, 8]. A typical language profile that has previously been observed in school-aged autistic children is relatively intact phonetic and syntactic (grammar) abilities, yet impaired semantics and morphology [e.g., 8, 9, 10, 11]. It should however be noted that even language skills generally considered intact appear to be differentially impaired in autistic populations [e.g., 12, 13, 14]. For example, Reindal et al. [13] demonstrated that 27% of their sample of autistic children between four and eighteen years old attained clinical scores on the syntax subscale of the Children’s Communication Checklist-2 (CCC-2) [15]. Additionally, autistic children, on average, produce less complicated sentences and wh-questions (e.g., questions with ‘who’, ‘where’, ‘what’, etc.) compared to their neurotypical peers, and sometimes struggle with reflexive pronouns (e.g., ‘himself’) [16, 17, 18].

Language deficits are not only prevalent in autistic children, but also in siblings with an elevated familial likelihood to develop autism (henceforth EL-siblings). Autism is highly heritable [19] and the recurrence rate for siblings of autistic children is close to 20% [20]. EL-siblings are therefore an often-studied population to examine early markers for autism, such as impaired language, even before the age a diagnosis can reliably be made. When the sibling at elevated likelihood is as young as six months old, some parents already express their first concerns about their child’s language development, regardless of whether the child eventually receives a clinical diagnosis of autism [21]. Additionally, a recent meta-analysis showed that even EL-siblings who did not receive a diagnosis were still three to four times more likely to exhibit language deficits or delays compared to siblings of neurotypical children [22], indicating that early delays in language may be an important behavioral endophenotype for autism.

While some studies have argued that language comprehension (receptive language) is more impaired than language production (expressive language) in autistic children and EL-siblings [e.g., 2, 23, 24, 25], a recent meta-analysis showed that, on average, receptive and expressive language are equally impaired, although individual differences are present [26].

Importantly, despite an ongoing debate about the similarities and differences between autism and developmental language disorder [see for example 2, 27, 28], language deficits and their underlying processes present in autistic persons cannot plainly be assumed identical to those in persons with a developmental language disorder [11, 25, 29, 30, 31 32]. Hence, language deficits of autistic children and EL- siblings cannot fully be explained by a comorbid developmental language disorder.

It remains unclear what does cause the heterogeneity of language abilities in autism. Many studies have investigated single factors impacting language development in autistic children and EL-siblings, such as motor skills [e.g., 33, 34], or parental language input [e.g., 35, 36], but a multifactorial risk model of genes, brain, behavior and environment seems more plausible than a single explanatory factor [37].

Better understanding of the heterogeneous pathways involved in shaping language abilities of autistic children and EL-siblings is crucial as language level, together with IQ, is one of the best-known predictors of post-childhood short- and long-term developmental outcome [e.g., 38, 39, 40, 41, 42, 43, 44, 45]. Conversely, language difficulties in childhood are associated with negative emotions [46], and low levels of functional ability in later life for autistic individuals [47].

This systematic review therefore aims to identify and summarize factors associated with receptive and expressive language development of autistic children and EL-siblings. The concept of “autism spectrum disorder” has only been formally introduced in the fifth edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-5) [4], and diagnostic categories and criteria have changed compared to the criteria for the pervasive developmental disorders in the previous versions in the DSM (DSM-IV-TR) [48]. Notably, references to atypical language development in diagnostic criteria present in the DSM-IV-TR have been omitted in the DSM-5, in which a comorbid developmental language disorder can be added as a specifier to the diagnosis. This makes a comparison of language abilities of children diagnosed based on differing diagnostic criteria between DSM-IV-TR and DSM-5 complicated. To ensure that results of this review consider only the most recent findings and do not reflect different diagnostic definitions [49] studies applying diagnostic criteria for “autism spectrum disorder” as specified by the DSM-5 will be considered or studies including siblings at an elevated likelihood for this condition.

A narrative review of factors influencing language abilities in EL-siblings has already been published [37], yet a systematic review that considers recent literature (since the formal introduction of the autism spectrum in the DSM-5) on factors associated with language abilities in autistic children and EL-siblings has not yet been conducted. Identifying factors that are linked to language development in autistic children is a first step towards defining the previously proposed notion of a multifactorial risk model for language deficits [37] and may ultimately shed more light on the heterogeneity of language abilities in these children. Knowing why some children develop language difficulties while others do not can potentially give insight into factors that put autistic children and EL-siblings at risk for developing language deficits, which can ultimately be informative for early, targeted interventions.

This literature review was performed in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [50].

Literature search

A comprehensive literature search to identify relevant articles was conducted on August 1^st and 2^nd 2021 and complemented by a final search close to the submission date on June 3^rd 2022. The search was limited to studies published in or after May 2013, when DSM-5 was introduced.

The online search was performed in Embase, MEDLINE, Web of Science Core Collection and Scopus. Within each database, keywords and subject headings pertaining to the following three broad concepts were used: (i) autism spectrum disorder; (ii) language development; (iii) pediatric sample. The terms in each category were included within parentheses using the Boolean operator “OR”, and the resulting four brackets were connected by “AND”. An overview of the specific terms used per database can be found in the search strategy in the supplemental information.

Inclusion and exclusion criteria

After the removal of duplicates, articles identified by the literature search were required to meet pre-established criteria to confirm their relevance. The inclusion and exclusion criteria were defined as follows:

Records had to include a retrospective, cross-sectional or prospective investigation into factors impacting receptive or expressive language skills in autism;
Participants were required to have an “autism spectrum disorder” diagnosis per DSM-5 criteria or had to be at an elevated likelihood for autism (EL-siblings);
The average age of participants in included records did not exceed six years and 11 months, when it can reasonably be expected that a child without notable developmental difficulties has mastered all milestones of their mother tongue, and variability in language skill is at its greatest [3];
The language measure used to characterize language abilities had to be reported explicitly. If this was not reported or if no language assessment took place, studies were excluded;
Records reporting the results of an intervention method were excluded;
Records focusing exclusively on second language acquisition and bilingualism were excluded;
Abstract-only papers (e.g., preceding papers, conference, editorial, and author response papers) were excluded;
Records were required to be published in English and in peer-reviewed journals;
Records without available full-text were excluded.

Search selection

An initial screening of records based on title and/or abstract took place by two independent reviewers (MM and SS). Records were included in a second screening if the title and abstract indicated that the article examined factors impacting receptive and/or expressive language abilities in autistic children and/or EL-siblings. Hereafter, full-texts were evaluated to check the inclusion and exclusion criteria. In the case of uncertainty about inclusion, the reviewers discussed the article and subsequently confirmed eligibility together. If it remained unclear if a record fulfilled the criteria, record authors were contacted for further clarification.

The electronic search was complemented by manually checking reference lists of included studies (backward chaining) and subsequent studies that cited the included papers (forward and backward chaining) on December 18 and 19, 2021. For a schematic overview of the review process, see Figure 1.

Data extraction

Of selected studies, crucial information was extracted of the overall sample and the sample per group if control groups were included. Information pertaining to sample size, average age of participants, gender ratio and socioeconomic status was collected as well as the main results of the study and the methods used, such as the operationalization of language skills. The first and second author independently extracted data from included reports and discussed the data in the case of uncertainty. This was the case for seven articles and was resolved among the authors for five of the articles. In the remaining two cases, the authors of the articles were contacted. Based on the information obtained from the authors, one of the articles was consequently included in the review [51] while the other was not. The detailed coding manual may be requested from the first author.

Study characteristics

A total of 54 articles drawing from 40 separate research studies were included in the systematic review (total study sample n = 3244 with autism, n siblings = 1379, 26% of the total study sample was female; sample size range = 8 – 1300; age range = 12.00 – 71.85 months at the time of language assessment). Fifteen studies used a cross-sectional design, the remaining 25 studies employed a prospective research design. 24 studies examined autistic children, 16 investigated EL-siblings. Some studies followed-up EL-siblings to the age at which diagnostic assessment was possible, in which case this information is provided. One study included minimally verbal autistic children [51]. In studies that provided information about SES and race, most participants were higher middle class and white.

A majority of 30 out of 40 studies (75%) exclusively included monolingual English-speaking children. Languages that were investigated in the remaining ten studies were Cantonese Chinese [52], Catalan [53], Dutch [54, 55], French [35], Italian [56], Korean [57], Mandarin Chinese [34, 58; 59), Spanish [53] and Turkish [60, 61].

Language abilities

The expressive and receptive subscales of the Mullen Scales of Early Learning (MSEL) [62], a standardized test of cognitive functioning, were most commonly used to characterize language abilities in included studies (n = 20 (50%)). Raw scores rather than standardized scores were often used in order to attain more variation in the data, since a floor-effect was frequently observed for autistic children and EL-siblings. Two other frequently-used measures were the MacArthur-Bates Communicative Development Questionnaire (M-CDI) [63], a parent-reported instrument to capture early language development (n = 16 (40%)) and the Vineland Adaptive Behavior Scales, 3^rd edition (VABS-III) [64], a tool to investigate children’s everyday adaptive functioning (n = 6 (15%)). Note that many of the included studies included multiple language assessments.

22 of the 54 included articles compared the language abilities of autistic children or EL-siblings with a neurotypical control group. Most of these articles (n = 17 (77%)) showed that autistic children and EL-siblings scored significantly lower on at least one of the employed language measures: one investigation showed lower general language abilities for EL-siblings without distinguishing between receptive and expressive language [65], two articles showed lower scores for EL-siblings only for receptive language [66, 67], three articles revealed lower scores for autistic children or EL-siblings only for expressive language [33, 68, 69] and 11 articles observed both lower receptive and expressive language abilities for autistic children or EL-siblings [34, 54, 55, 70, 71, 72, 73, 74, 75, 76, 77]. The remaining five articles did not identify group differences [35, 56, 78, 79, 80].

Factors implicated in language

The systematic literature review identified a total of 56 factors that were significantly associated with language abilities in autistic children and EL-siblings. 13 factors were only investigated in broad language abilities without differentiating between receptive or expressive language; 17 and 36 factors were identified for receptive language and expressive language, respectively. Some factors were associated with both receptive and expressive language abilities. It should however be noted that studies more frequently considered expressive language abilities compared to receptive abilities. Receptive language abilities were exclusively investigated with standardized tests. These instruments generally included an expressive measure as well. Thus, when receptive language was investigated, expressive language was almost always also investigated with the same instrument. On the other hand, isolated expressive language abilities (e.g., mean length of utterance, expressive vocabulary etc.,) were often examined using (semi-)spontaneous language samples, for example acquired during parent-child interactions, where receptive language abilities were generally not additionally assessed. This leads to only one study investigating receptive language abilities [81], while 13 studies uniquely considered expressive language abilities. An overview of the 56 factors and their involvement in receptive and expressive language abilities can be found in Table 1.

The large table including all study characteristics and main results can be found in Table 2 in the Appendix.

We divided the established language-associated factors into 10 categories: autism traits; biological factors; brain-based factors; child characteristics and early child development; environmental factors; gestures; motor skills; parental input; social factors; other factors.

Table 1

Summary of factors associated with receptive and/or expressive language in autistic children and EL-siblings
	Receptive language	Expressive language	General language abilities
Autism traits
Hypo-reactivity to sensory stimuli			1
Restricted and repetitive behaviors	1
Severity of social communication impairments	2	1
Biological factors
Biological sex			2
Brain-based factors
Cortical reactivity	1
Fractional anisotropy in the inferior longitudinal fasciculus	1	1
Frontal delta power			2
Frontal high-alpha power		2
Frontal theta power			2
Gamma power		2	2
Greater signal increases in the left Heschl’s gyrus and superior temporal gyrus (speech processing)		1
Left frontal-central alpha coherence		1
Neural correlates of face processing	1	1
P3 peak latency		1
Surface area left rostral middle frontal gyrus			1
Speech evoked auditory brainstem response			1
Temporal gamma power		1
Child characteristics & early child development
Early child vocalizations		1
Initial child language abilities		2
Nonverbal cognition	2	3
Environmental factors
Maternal education*	1	1
Serum folate levels			1
Gestures
Child gesture quantity	1
Child gesture type		1
Maternal gesture use			1
Parental gesture quantity		1
Parent gesture type		1
Motor skills
Composite score motor skills	2	2
Fine motor skills	1	2
Gross motor skills	1	1
Motor imitation ability		1
Postural control	1	1
Parental input
Maternal mean length of utterance		1
Parent mean length of utterance	1	1	1
Parent verbal responsiveness			1
Paternal verbal responsiveness			1
Use of telegraphic speech	1
Social factors
Attention to synchronous over asynchronous videos			1
Frequency of other-directed vocalizations		1
Increased attention to eyes and face		2
Increased attention to mouth		1
Intentional communication		1
Joint attention	4	2
Larger latency to respond			1
Object imitation		2
Object play		1
Percentage simultaneous speech between parent and child			1
Preference for speech over non-speech		1
Relative preference for faces over objects		1
Social motivation		1
Social responsiveness	1	1
Symbolic comprehension		1
Other
Ability to map differentially stressed labels to objects		1
Mother rigidity (BAP traits)			1
Speech production abilities		1
Use of mutual exclusivity in word learning	1
Note: Numbers refer to the number or articles in which each factor was found to be significantly related to one or more language measures. *This effect was rendered insignificant after correcting for multiple comparisons

Autism traits. Autism traits, specifically the severity of social communicative difficulties, restricted and repetitive behaviors, and hyporeactivity to stimuli were investigated in four included articles [54, 57, 82, 83]. For autistic children, the severity of social communication impairments was negatively associated with receptive and expressive language in one study investigating six-year-old children [57], but not in a second study investigating autistic preschoolers [83]. This second study also did not find significant effects of restricted and repetitive behaviours on the language abilities of autistic children.

In EL-siblings, both the severity of social communication impairments and restricted and repetitive behaviours did seem to have an effect, as they were negatively associated with receptive language growth, but not expressive language growth between 10 and 36 months [54]. Note that in this study, five out of 31 EL-siblings would later receive a diagnosis and eleven were found to present with the broader autism phenotype.

Lastly, it was established that hypo-reactivity to sensory stimuli at fourteen months was negatively related to language abilities at 23 months in EL-siblings [82]. This effect was however fully mediated by parental verbal responsiveness, meaning that increased parental responsiveness may attenuate negative effects on language associated with hypo-reactivity to sensory stimuli [82]. In this study, 34% of the EL-siblings who were available for a preschool follow-up received a diagnosis.

Biological factors. Only two studies, with conflicting results, examined a biological factor, namely biological sex, both in a sample of autistic children [84, 85]. One study [85] reported that parents indicate fewer language concerns for autistic females compared to autistic males (respectively 55.6% and 72.4%), while the other [84] found that autistic females were more likely to have greater language impairment compared to autistic males. Operationalization of language may play a part in the diverging results: one study examined only current expressive language-levels [85], while the other investigated both present and past parent concerns about receptive and expressive word-level difficulties [85].

Brain-based factors. Brain-based factors were most frequently investigated in samples involving EL-siblings, as many of the included papers here draw from the same overarching research study (the Infant Sibling Project) [e.g., 74, 77]. Two included research articles however examined children with an established diagnosis.

Using structural MRI, Chen et al. [58] investigated the role of the speech-evoked auditory brainstem response (speech-ABR) and broad language abilities in three- to six-year-old autistic children. The speech-ABR is a neurological test to evaluate the auditory brainstem function in response to auditory stimuli [86, 87]. The authors classified participants into subgroups based on their speech-ABR to complex sounds, which was either typical or atypical. Autistic children with an atypical speech-ABR had significantly lower language scores than those with a typical response. Moreover, for all autistic children, the surface area of the left rostral middle frontal gyrus, part of the dorsolateral prefrontal cortex, had an indirect effect on language via the wave V amplitude, a wave generated in the upper brainstem as a response to an auditory stimulus, which, as Chen et al. [58] propose, suggests that subcortical dysfunction caused by cortical deficits may impair language ability in autistic children.

The second study utilized diffusion tensor imaging (DTI) to examine their sample of three-year-old autistic males, and established that fractional anisotropy, a measure of connectivity that evaluates white matter, in the occipital portions of the left and right inferior longitudinal fasciculus, a pathway between the occipital and temporal lobes, was positively linked to both expressive and receptive language [88].

As for EL-siblings, multiple articles, many drawing from the same longitudinal study sample, examined frontal EEG power in different frequency bands during a resting-state task. The intercepts of frontal delta, gamma and theta power at six months old were significantly associated with broad language abilities at 24 months, both in EL-siblings who would go on to receive a diagnosis and those who did not [77, 65]. Interestingly, the direction of the effect of frontal gamma power was reversed for EL-siblings who received a diagnosis and those who did not: whereas for this first group high gamma power at the age of six months was associated with lower language scores, for EL-siblings without eventual diagnosis, it was related to increased language ability [77].

When distinguishing between receptive and expressive language, increased frontal gamma power was established to be negatively related to expressive language for EL-siblings regardless of later diagnostic status, but not for those at typical likelihood [77]. This effect was however largely driven by females, underscoring the importance of including biological sex in analyses [77]. Frontal high alpha power was also positively associated with expressive language for EL-siblings with and without a later diagnosis and siblings of neurotypical children [69], as was left frontal-central alpha coherence, a measure of connectivity [75, not part of the Infant Sibling Project].

Gamma power was investigated as a mediator in the relation between parental language input and child language abilities [74]. Parent-child interaction was used to characterize the quality and quantity of parental input when children were 18 months old and relations with expressive and receptive language at 24-months old were investigated. An association was found with expressive language for the whole sample (siblings of autistic and neurotypical children), but only for EL-siblings who would ultimately go on to receive a diagnosis, the effect was mediated by frontal and temporal gamma power [74]. Moreover, replicating previous results of Wilkinson et al. [77], gamma power had a direct negative effect on expressive language scores in for the whole sample, but especially for EL-siblings that received a later diagnosis.

Glauser et al. [89], also drawing from the sample of this larger research study, investigated the neural correlates of face processing and their impact on receptive and expressive language. Using event related potentials (ERPs), they showed that an increased P400, an ERP sensitive to face processing, response to a picture of the EL-siblings’ mother over a picture of a stranger was positively associated with receptive and expressive language abilities of EL-siblings that would later receive a diagnosis, but not for EL-siblings without later diagnosis or siblings of neurotypical children [89].

In two other EEG studies investigating EL-siblings, an auditory oddball task was used [56, 90]. With this paradigm, children heard a sequence of ‘standard’ stimuli, in which a different stimulus was occasionally and seemingly randomly introduced. Studying ERPs related to auditory processing, one study showed that P3 peak latency, an ERP assumed to be a measure of time needed to evaluate and categorize a stimulus [91], was significantly delayed in EL-siblings and in children with an elevated likelihood of developmental language disorder, and this longer latency was negatively associated with expressive vocabulary in the whole sample [56]. The second study investigated cortical reactivity and demonstrated that for all children in the sample (EL-siblings and neurotypical children), higher cortical reactivity at nine months was associated with reduced receptive language growth between eight and 36 months. No significant effects were observed for expressive language [90].

Lastly, a functional MRI study investigating neural sensitivity to speech prosody indicated that for EL-siblings, a greater signal increase during speech stream exposure in the Heschl’s gyrus was associated with better expressive language scores at 36 months [92]. The Heschl’s gyrus contains the primary auditory cortex and the superior temporal gyrus, which includes Wernicke’s area and is involved in auditory processing. Interestingly, an fNIRS study examining neural correlates of speech processing did not observe an impact on language abilities in EL-siblings, although there was a positive effect on language in neurotypical children [93].

Child characteristics & early child development. One often investigated child-related predictor for language abilities was nonverbal cognitive abilities [52, 53, 54, 83]. Torras-Mañá et al. [53] investigated the association between nonverbal cognitive abilities and expressive language abilities in four-year-old Spanish and Catalan speaking autistic children. They revealed a significant association between nonverbal cognitive abilities and later oral language, with 72% of the children with poor early nonverbal cognitive abilities remaining minimally verbal and 82% of children with typical early nonverbal cognitive abilities attaining phrase-level to fully fluent verbal language at the age of four years old. Nevill et al. [83] replicated this positive association between nonverbal cognitive abilities and expressive and receptive language in autistic children. They also state that autistic children with typical nonverbal cognitive abilities were, however, still at risk of developing language impairments [83], indicating that low nonverbal cognition cannot be the only explanation for the impairments.

One study did not establish a significant association between nonverbal cognition and language in autistic children [52]. This discrepancy may be due to differences in sample age, as participants in Song and So’s study were, on average, over a year older at the time point of language evaluation compared to participants in the other studies, or to differing language assessments, with Song and So [52] utilizing a spontaneous speech sample to characterize expressive language and the other authors employing standardized language tests [53, 83]. Previous research has indicated that autistic children show significantly more impairments on spontaneous language measures compared to standardized tests, but these results should be interpreted with caution due to the lack of psychometric norms for spontaneous language approaches [94].

Other factors relating to child characteristics and early development that were identified were initial child language abilities [52, 53] and frequency of early child vocalizations [95] (independent of communicative intent, for other-directed vocalizations see Social factors), all of which were found to be strongly and positively associated with later expressive language abilities in autistic children.

For EL-siblings, only nonverbal cognitive abilities were investigated. Similar to the results in autistic children, for EL-siblings a significant positive association with both expressive and receptive language was confirmed [54]. Note again that in this study, five out of 31 EL-siblings received an eventual diagnosis and 11 were found to present with broader autism phenotype.

Environmental factors. Two environmental factors were identified: serum folate blood levels [59] and socioeconomic status [73]. Both were only investigated in autistic samples.

Serum folate is derived from dietary sources and low levels of serum folate have been previously linked to developmental disorders [96]. In the study of Li et al. [59], autistic children (n = 1300) exhibited lower serum folate levels compared to neurotypical children, potentially due to feeding problems (e.g., being a picky eater, reduced vegetable intake). Higher serum folate blood levels were associated with better general language abilities, but only in children three years and younger. The authors state that associations of serum folate levels may differ per age, as clinical manifestations of autistic children differ over time too [59].

Olson et al. [73] examined the association between multiple factors pertaining to SES, specifically household income, maternal and paternal education level and median neighborhood SES by postal code and expressive and receptive language. The results show that maternal education was significantly related to parent-reported and clinician-rated receptive language, and parent-reported expressive language abilities for the entire sample (autistic and neurotypical children), with lower maternal education indicating lower child language abilities. These results were however rendered insignificant after controlling for multiple comparisons.

Gestures. Both parent gestures and child gestures appear to impact language abilities in autistic children and EL-siblings. For autistic children, gesture type was investigated. It was found that declarative gestures (gestures to direct a person’s attention to something the child finds interesting) and conventional gestures (gestures that are symbolic, such as waving hello), but not imperative deictic gestures (pointing to direct another person’s attention to obtain a goal) were significantly associated with expressive language in both autistic and neurotypical children [60].

For EL-siblings, gesture frequency was of importance. The frequency of gestures significantly predicted receptive, but not expressive language scores at 24 months in siblings with and without elevated likelihood, regardless of later diagnostic status [97]. Not only child gesture frequency, but also parent (mostly mother) gesture frequency played a role for these children, as frequency of their gesture use was found to be related to later expressive language abilities of their children, both for EL-siblings with and without later diagnosis and siblings of neurotypical children [98]. The type of gestures parents used was important too, as specifically declarative gestures and conventional gestures, but not imperative gestures predicted expressive language across the sample [67]. Furthermore, maternal gesture use specifically impacted broad language abilities in EL-siblings without a later diagnosis and siblings of neurotypical children, but not in EL-siblings who went on to receive a diagnosis at the end of the longitudinal study [80].

Motor skills. Several aspects of motor abilities and their relation to language abilities were investigated, especially in EL-siblings. One included study that examined autistic children, showed that a composite score of motor abilities was significantly related to receptive and expressive language, with lower motor skills resulting in lower language scores and vice versa [34]. These results were replicated in EL-siblings, but the effects were partially mediated by joint attention, as motor skills impacted the ability to execute joint attention behaviors (e.g., object sharing), and joint attention in turn affected language abilities [55]. Note that of the sample of 32 EL-siblings, six ultimately received a diagnosis and 11 presented with broader autism phenotype.

When investigating motor skills in EL-siblings further, one longitudinal study showed that fine motor skills specifically were significantly and positively linked to expressive language abilities in the whole sample [33]. Siblings who went on to receive a diagnosis obtained significantly lower fine motor scores compared to siblings who would not [33]. These results were replicated by Patterson and colleagues [99] who found that early fine and gross motor trajectories from six to 24 months were correlated with receptive and expressive language abilities at 36 months old in EL-siblings with and without eventual diagnosis. Their results show that flatter developmental trajectories of motor abilities were related to lower language scores, whereas accelerating trajectories were associated with higher language scores [99].

Edmunds et al. [78] investigated motor imitation abilities and later parent-reported expressive language abilities in EL-siblings. Significant effects were observed indicating that better motor imitation abilities were related to better expressive language outcomes for EL-siblings and siblings of neurotypical children. Similar to Bruyneel et al. [54], the effect was mediated by response to joint attention [78]. Note that diagnostic status of the children in this study was unknown as participants were still too young for reliable assessment at the end of the study.

In contrast to the above results, one study examining fine motor skills and its relationship to expressive and receptive language in EL-siblings indicated that although fine motor and language pathways correlated highly over time, the two skills were not coupled, as differences in children’s baseline fine motor abilities did not affect the growth rate of language abilities (receptive and expressive) [100]. This was the case for both EL-siblings who would later receive a diagnosis as well as for those who would not [100].

Lastly, the role of postural control at six months of age and later expressive and receptive language at twelve months was explored in a sample of eight EL-siblings [72]. The results indicate that EL-siblings who had faster control over their posture, had significantly higher receptive language scores, and that “steady sitters” (i.e., children with low random movement) had better receptive and expressive language outcomes. EL-siblings included were still too young for formal assessment of their diagnostic outcome.

Parental input. Three included articles investigated the influence of parental input on the language abilities of autistic children [35, 102, 103]. Based on parent-child interactions, Flippin et al. [103] investigated mothers’ and fathers’ verbal responsiveness and the relationship with broad language abilities of autistic children. They demonstrated that only the frequency of fathers’, and not mothers’, verbal responsiveness, appeared to be associated with child language scores in their sample of children with ASD [103].

Another indexation of parental input is the parent mean length of utterance (MLU). In their study, Bang and Nadig [35] showed maternal MLU to have a positive effect on the expressive language abilities of both autistic and neurotypical children.

Lastly, the role of parent telegraphic speech on autistic children’s expressive language abilities was studied. Telegraphic speech describes an expressive language style focused on content words, often omitting adjectives, articles and other grammatical morphemes. Although a natural stage in all children’s language development, it is sometimes adopted by parents of autistic children as some clinicians recommend this technique for language learning for these children [101]. Venker et al. [102] explored parent use of telegraphic speech during parent-child interactions and expressive language levels. They demonstrated that parent use of telegraphic speech at three years negatively impacted the number of different words used by autistic children one year later, even after controlling for initial language levels and nonverbal cognitive ability, and that telegraphic language input may discourage imitation of grammatical utterances, hence potentially preventing children from learning new words through syntactic bootstrapping.

For EL-siblings, similar results were found. One article showed that also for EL-siblings parent verbal responsiveness at fourteen months directly impacted broad language abilities at 23 months [82]. In this study, 34% of the EL-siblings who participated in the study and were available for a preschool follow-up ultimately received a diagnosis.

Apart from parental verbal responsiveness, significant positive effects for parental (mostly maternal) MLU at twelve and eighteen months on general language abilities [70] and expressive and receptive language specifically [74] have been observed for EL-siblings one year later, even after controlling for parental education, family income and initial child language levels [70, 74]. These results hold for both EL-siblings who went on to receive a diagnosis and for those who did not, but no significant effects were found for siblings of neurotypical children [70, 74].

Social factors. Social factors were amongst the most frequently identified variables in the included articles and were mostly related to expressive language rather than receptive language. One important variable investigated in the context of social factors was joint attention, although mixed results were observed. One longitudinal study found significant, positive associations between joint attention and expressive language growth and baseline receptive language in autistic children [104] while two other studies found significant effects for autistic children’s receptive language only [83, 105]. Joint attention was also examined in EL-siblings. Here too, mixed results arose as one study found a significant association with receptive language only [55] and another with expressive language only [78], regardless of later diagnostic status. With five different studies exploring the role of joint attention in shaping language abilities, it is the best examined factor identified.

Furthermore, two eye-tracking studies examined attention to the face during videos of a person talking in an autistic sample. It was shown that attention to the eyes and mouth over other facial features was related to better language scores in both autistic and neurotypical children [106]. In the same study, differential sensitivity to speech processing was examined by showing autistic and neurotypical children videos of a woman speaking, either with synchronous or asynchronous audio [106]. The authors showed evidence that attention to synchronous over asynchronous videos was related with better language abilities for both autistic and neurotypical children [106].

Another study found that looking at the mouth over looking at the eyes was significantly and positively related to expressive language in 20-month-old autistic children who had already acquired first words, but not for autistic children who had not yet acquired speech at the same age, or neurotypical children [71].

Other factors examined in autistic children were frequency of other-directed vocalizations [83], object imitation skills [61, 104], object play [61], parent-rated social motivation [107] and social responsiveness and symbolic comprehension [105]. Nevill et al. [83] found a positive association between the frequency of other-directed vocalizations and expressive language abilities of autistic children. Frost et al. [104] and Şengül et al. [61] also observed a significant positive relation between expressive language and object imitation skills. However, this effect disappeared when joint attention was added to the model, suggesting that object imitation does not provide unique variance in the prediction of expressive language abilities [104]. Object play (play complexity with different toy sets) was related to expressive language too, as children who received better scores for object play (and thus showed more complexity), were less likely to be minimally verbal [61].

Social motivation (i.e., the motivation to engage in social communication) was also related to expressive language, but this effect was mediated by intentional communication, indicating that autistic children with stronger social motivation were more likely to frequently produce instances of intentional communication, in turn leading to better expressive language abilities [107]. Symbolic comprehension, a term referring to the ability to understand social communication, such as gesture use, was related to the expressive language abilities of autistic children, with poor symbolic comprehension indicating lower expressive language levels [105]. Social responsiveness (i.e., the response of the child to the emotional expression of the clinician) was related to both expressive and receptive language in autistic children [105].

When examining EL-siblings, one eye-tracking study showed that a relative preference for faces over objects resulted in higher expressive language scores in EL-siblings, but not in siblings of neurotypical children [68]. Later diagnostic status of the EL-siblings in this study is unknown as children were too young to undergo formal assessment by the end of the study. Another eye-tracking study revealed that, similar to autistic children, increased attention to the eyes and face over looking at the mouth in six-month-old EL-siblings, independent of later diagnostic status, had a negative effect on expressive, but not receptive language at eighteen months old [76]. Eight of the 37 EL-siblings participating in this study would go on to obtain a formal diagnosis. Interestingly, another eye-tracking study found no significant effects of preferential attention to specific facial features on expressive nor receptive language for EL-siblings without later diagnosis [66].

Another factor positively associated with expressive language abilities in EL-siblings was a preference for speech over non-speech stimuli [108].

Three factors were only explored for EL-siblings’ broad language abilities in Northrup and Iverson [79]: the percentage of simultaneous speech between parent and child, a larger latency to respond to one another during parent-child interactions and a preference for synchronous videos over asynchronous speech videos. The amount of simultaneous speech between parent and child (i.e., the amount that both spoke at the same time), was indicative of later language delay, and a larger average latency to respond to one another occurred significantly more often in EL-siblings with comorbid language delay [79]. The study did not differentiate between the later diagnostic status of EL-siblings. Note that the effects of joint attention for EL-siblings were already discussed above, in the paragraph concerning autistic children.

Other factors. We identified four additional factors with an impact on language abilities of autistic children and siblings that did not fit the above categories, namely broad autism phenotype (BAP) traits in parents [109], speech production abilities [51] and the use of mutual exclusivity in word learning [81] and, for siblings, the ability to map differentially stressed labels to objects [112].

Flippin et al. [109] examined the presence of BAP traits in parents using the Broad Autism Phenotype Questionnaire (self-report) [110] in relation to the language abilities of autistic children. This questionnaire contained questions related to three subscales reflecting ASD characteristics: aloofness, rigidity and difficulties with pragmatic language. Only mother rigidity had a significant impact on child language abilities, even after controlling for their verbal responsiveness. This result may be indicative of a stronger history of interaction between children and their mothers compared to fathers, as almost all mothers participating in the study identified as the primary caregiver.

Saul and Norbury [51] investigated diverse aspects of minimally verbal children’s phonetic repertoire and their impact on expressive language. Their results show that speech production abilities at an average age of four years significantly predicted expressive language one year later. The authors suggest the presence of a potential additional speech-sound production deficit in minimally-verbal autistic children that contributes to the deficits in expressive language.

Lastly for autistic children, Mathée-Scott and colleagues [81] investigated the use of “mutual exclusivity” in an eye-tracking task and its relation to receptive language abilities. Mutual exclusivity is a strategy for word learning in which the child maps a novel label to a novel object and not to an object they already have a label for [111]. The authors show that autistic children who appear to struggle with the mutual exclusivity strategy, have significantly lower receptive language abilities than those that do correctly apply this strategy.

For EL-siblings, the ability to map differentially stressed labels to objects was shown to play a role in their language abilities. This entails the ability to use linguistic cues such as prosody and stress to match unfamiliar words to objects, thus facilitating word learning. In a longitudinal study exploring this ability in EL-siblings, success on an experimental task at twelve months old, indicating successful mapping of labels to objects, predicted better expressive language abilities one year later. This was however not the case for siblings of neurotypical children. For these children success on the task was only related to current language comprehension [112].

An overview of all discussed factors is shown in Table 1.

Risk of bias and quality assessment

Risk of bias of eligible articles was assessed with the Newcastle-Ottowa Scale (NOS) for case-control studies [113]. The NOS employs a star rating system assessing three broad categories: selection of study groups and, for studies including a control group, comparability of groups and ascertainment of the outcome. Between zero and nine stars can be awarded to each article, the more stars a study receives, the lower the risk of bias. The first and second authors independently assessed the risk of bias of all included studies. Any discrepancies in ratings were resolved among the reviewers by discussion. The risk of bias varies from low to high risk and is summarized in the appendix in Table 3.

In order to take a first step towards defining a multifactorial risk model for language deficits in autism [37], we identified 56 factors from recent literature that were significantly implicated in receptive and/or expressive language abilities in autistic children and EL-siblings (see for an overview Table 1) and assigned them to ten broader categories (autism traits; biological factors; brain-based factors; child characteristics and early child development; environmental factors; gestures; motor skills; parental input; social factors; other factors). We found that, on average, autistic children and EL-siblings obtained significantly lower receptive and expressive language scores than their neurotypical peers. These results are in line with a rich body of evidence showing that expressive and receptive language deficits are highly prevalent in autistic children and EL-siblings [3, 14, 21, 26].

Towards a multifactorial risk model

Our results make apparent that no single factor alone can explain the heterogeneity in language abilities of autistic children and EL-siblings. Although our findings are scattered, as most implicated factors were only investigated in a single study, we did identify some similarities across studies. Especially joint attention was frequently shown to be associated with receptive language [54, 83, 104, 105] and expressive language [78, 104), with the presence of joint attention behaviors being linked to better language skills. This is in line with previous work indicating that joint attention abilities are important for emerging language, and delays or absence of these behaviors is related to lower language abilities and language delays [e.g., 23, 114].

Apart from joint attention, other social factors, especially relative attention to specific facial features of others, were primarily implicated in expressive language [71, 76 106]. These findings confirm prior work establishing evidence that social factors predict expressive language abilities in autistic children [e.g., 115, 116, 117]. However, the fact that we found more factors associated with expressive language than receptive can in part be attributed to a higher number of studies focusing on expressive language.

Child characteristics such as nonverbal cognition and initial child language abilities were recurrently positively associated with both receptive and expressive language abilities [52, 53, 54, 83]. Children with typical or above typical nonverbal cognition were less likely to have language deficits [53, 83]. (Above) average nonverbal cognition may thus serve as a protective factor for language deficits in autistic children and EL-siblings. Hence, (early) verbal language, cognition and social impairments seem a promising facet in further delineating a risk model, especially for expressive language abilities.

Other promising behavioral components for the further delineation of a risk model are autism traits and motor abilities. Autism traits are likely to play a role in language, as mainly impairments in the social communication were negatively related to expressive and receptive language [54, 57]. Well-developed early motor abilities in autistic children and EL-siblings were shown to be related to better later language abilities [33, 34, 55, 72, 78]. It remains unclear however if there is a direct effect of motor skills on language, or if this relationship is mediated by other variables, such as joint attention.

Lastly, exploring a neurocognitive component, different brain-based elements appeared to be of importance. Especially frontal EEG power (in alpha, delta, gamma and theta bands) during the first year of life was frequently investigated and partly predicted later expressive language abilities in EL-siblings [65, 69, 74, 75, 77). It should however be taken into account that most included investigations were part of a larger overarching research study and thus examined the same sample [65, 67, 69, 74].

While we have identified many different overarching categories that are likely to play a role in shaping language abilities in autism, the role of genetics remains underexposed. Throughout the literature search, we did not encounter studies compliant with our inclusion criteria that investigated the role of genetics on language abilities in young autistic children or EL-siblings. As autism itself has a large genetic component [e.g., 118, 119, 120], investigating genes in the context of language abilities in autistic children and EL-siblings seems a compelling avenue for future research.

Differences and similarities between children with and without autism

There appears to be substantial overlap in the factors implicated in language abilities between autistic children and EL-siblings on one hand and neurotypical children on the other [e.g., 35, 60]. Where differences were observed, they could often be at least partially explained by factors inherent to autism. For example, the frequency of restricted and repetitive behaviours was negatively associated with receptive language in EL-siblings, but not in siblings of neurotypical children [54]. The frequencies of these behaviors were significantly higher in EL-siblings, as they make up a crucial part of autism. This increased frequency may have a relative negative effect on language abilities, but absence of restricted and repetitive behaviors may not be of importance for language abilities. Unfortunately, many studies did not have large enough samples to investigate autistic and neurotypical groups separately. This is even more so the case for distinguishing groups of EL-siblings with and without eventual diagnosis. More research in larger samples, and consequently more power, is necessary.

Mixed findings and language assessment

Mixed results were frequently present in the literature (e.g., for biological sex [84, 85] and speech processing [92, 93]). Part of these mixed, sometimes contradictory, findings may lie in the fact that studies used vastly different measures to assess language abilities, which underscores the need for uniform language assessment to make cross-study comparisons possible. Some studies included in this review employed a (semi-)spontaneous language sample, which, though time consuming to analyze, provides a more naturalistic and informative impression of the child’s expressive language abilities and seems feasible to assess in a large part of children on the autism spectrum. However, standardized approaches with well-established norms for different age groups and different languages are currently lacking for spontaneous speech samples, making it difficult to establish cut-offs for language impairments.

Limitations of the current review

Certain limitations of the current review should be considered. First, this work focuses exclusively on children with a diagnosis of autism spectrum disorder as characterized by DSM-5 criteria [4] and EL-sibs. This inevitably led to the exclusion of many meaningful research articles and, considering the overlap between previous and current diagnostic criteria, we have therefore likely missed important results. For example, Lombardo and colleagues authored several papers regarding MRI-data and language outcomes in autistic children [e.g., 121, 122, 123], that unfortunately fell beyond the scope of the current literature review as the children in their sample were diagnosed based on the DSM-IV-TR [48], which served as an exclusionary criterium here.

A second limitation of this review is that the average age of participants in included records could not exceed six years and 11 months. This age limit was chosen as language milestones are typically long achieved by age six, and as previous research has shown that after this age variability in language skill becomes surprisingly uniform [3]. Taking advantage of the high variability in language abilities in the years before, this age range is an ideal window to evaluate language differences between autistic and neurotypical samples and the factors impacting these differences. However, to gain a full overview of language development and a potential developmental shift in factors implicated in language abilities, older age groups until adolescence should be given attention. Additionally, this review deliberately focuses on broad abilities in expressive or receptive language, but more fine-grained language processes, such as syntactic comprehension (e.g., quantifier processing) may ultimately shed more light on underlying cognitive processes of language that may or may not differ between those with and without autism. Such processes can often only be studied in older children given their age of acquisition.

Lastly, more general limitations that are frequently present in autism research should be acknowledged. Autistic children included in the samples discussed here likely only represent part of the autism spectrum, as some children would be unable to participate in the testing sessions of included studies. Especially those with high support needs may not be able to participate in research settings and are therefore often not included. This may in turn result in cascading high language scores in current research samples that do not reflect the entirety of the autism spectrum. Additionally, generalizability of our results should be interpreted with caution as most studies included relatively small samples representing predominantly white, monolingual English-speaking children from middle to high socioeconomic backgrounds.

We identified several factors that were associated with receptive and expressive language abilities in autistic children and EL-siblings in an effort to further delineate a potential multifactorial risk model for language impairments in autism. We found several promising facets for such a model, such as joint attention, nonverbal cognition, early child language abilities, social factors and motor abilities, but more research is necessary, as several potentially valuable components, such as a genetic one, are largely unexplored in young children. Further investigating risk factors and protective factors for language impairments in autistic children and EL-siblings may contribute to the development of early language intervention methods that in turn can help prevent or counteract negative adversities associated with reduced language abilities.

Funding

This work has received support from the EU/EFPIA/SFARI/Autistica/AUTISM SPEAKS Innovative Medicines Initiative 2 Joint Undertaking (AIMS-2-TRIALS grant n° 777394). Any views expressed are those of the author(s) and not necessarily those of the funders.

Conflicts of interest

The authors have declared no competing interests.

Availability of the data and material

The detailed coding manual can be requested from the first author.

Code availability

Not applicable

Ethics and informed consent

Not applicable

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Factors Associated with Receptive and Expressive Language in Autistic Children and Siblings: A systematic review

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