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. Author manuscript; available in PMC: 2024 Jul 26.
Published in final edited form as: Volta Rev. 2023;123(1):1–20.

Hearing, Speech, and Language in Infants and Toddlers Born Prematurely

Lisa L Hunter 1,4, Jennifer Vannest 1,5, David R Moore 1,4, Maria Barnes-Davis 2,3, Chelsea Blankenship 1, Lauren Prather 1,5, Jody Caldwell-Kurtzman 1, Nehal Parikh 2,3
PMCID: PMC11281542  NIHMSID: NIHMS1954075  PMID: 39070928

INTRODUCTION

Worldwide, 15 million babies are “born too soon” every year (Blencowe et al., 2012; Howson et al., 2013). Remarkably, prematurity survival rates now exceed 93% across all countries. More than 360,000 preterm babies survived in the US in 2020; 10% of all births (Blencowe et al., 2012; Howson et al., 2013). While this is an incredible achievement, preterm birth places the developing infant in a particularly vulnerable state for life-long adverse developmental outcomes. Due to improved survival rates, developmental disabilities, including hearing, visual, motor, cognitive, speech-language and literacy deficits have also increased (McCormick & Behrman, 2007). In addition to the medical and developmental consequences, the increased cost of raising a preterm child compared to a term-born child exceeds $134,000 or >60 billion annually in US dollars, adjusted for year 2023 (Mangham et al., 2009). In contrast, the cost of early intervention is a relative bargain, at $1240 per preterm infant, adjusted for year 2023 (Clements et al., 2007). Effectiveness of early intervention is highly likely to be effective, based on the remarkable plasticity of the newborn brain (White et al., 2013).

Speech-Language Development and Prematurity

Speech and language disorders are among the most prevalent neurodevelopmental disorders in children, with prevalence rates in the range of 5–8% of all preschool children (Law et al., 1998; Tomblin et al., 1997). In contrast, about 40% of very/extremely preterm infants (≤32 weeks gestational age) develop persistent speech-language disorders (SLD) (Duncan et al., 2012; Nguyen et al., 2018). Based on prevalence estimates, about 40,000 very-extremely preterm babies (≤32 wks. gestational age, hereafter referred to as preterm) develop SLD (Duncan et al., 2012; Nguyen et al., 2018) annually in the US. Accurate identification of SLD in children born premature often does not occur until age 3–5 years, and persists in about 2/3 children (Roulstone et al., 2003) placing them at high risk for life-long poor educational, vocational, and social outcomes (Bashir & Scavuzzo, 1992; Young et al., 2002). Currently, it is not possible to accurately predict in the first year of life which children will develop SLD. As a result, speech-language therapy is the most delayed and the least common of the therapy services provided to infants after Neonatal Intensive Care Unit (NICU) discharge (Nwabara et al., 2017). Precious time is lost during the first three years, in which intervention is most effective, resulting in increasing speech, language and reading deficits at school age (Vohr et al., 2018; Vohr, 2016). Our research program is informed by longitudinal studies (Fig. 1) in preterm children that show typical language development in 32%, delay that resolves over time in 28%, and persistent/increasing delay in 40% (Duncan et al., 2012; Nguyen et al., 2018), who need early identification and intervention.

Figure 1.

Figure 1.

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Developmental trajectories in prematurity (P), in relation to speech-language and literacy outcomes (S-L): Measures include Brain connectivity/processing (B); Hearing loss (H). Three trajectories are shown: Normal (Green line); Resilient (Blue line) and High Risk for SLD (Orange line).

Hearing Loss and Prematurity

Overall, ten times as many preterm compared to term babies have some degree of permanent hearing loss (Hirvonen et al., 2018; Robertson et al., 2009), compounding the impact on communication difficulties (Hirvonen et al., 2018; Robertson et al., 2009). Prevalence estimates for hearing loss varies widely due to variable diagnostic criteria and risk factors, e.g. brain injury, prenatal infections, hyperbilirubinemia and exposure to drugs that are toxic to the ear (Cristobal & Oghalai, 2008). Preterm birth can also result in delayed or progressive hearing loss, additionally contributing to SLD (American Academy of Pediatrics, 2007). These delayed and progressive hearing losses may occur due to ongoing problems related to premature birth and these various risk factors (JCIH, 2019). Current methods of Newborn Hearing Screening (NHS) reliably only detect hearing loss greater than 30–40 dB HL, thus missing most slight-mild and higher frequency loss (Garinis et al., 2018). Even mild and high frequency hearing loss increases the risk for SLD (Walker, Holte, et al., 2015; Walker, McCreery, et al., 2015). These so-called “minimal” losses are related to poorer language outcomes (Porter et al., 2013; Walker, McCreery, et al., 2015; Winiger et al., 2016) and are at least 3 times more prevalent than moderate/greater loss (Su & Chan, 2017; Vohr, 2016). In a large primary school cohort (n=1638), Moore and colleagues reported that prevalence of undiagnosed slight-mild hearing loss (15–25 dB HL) was 16.8%, and was significantly associated with poorer language, word and nonword repetition, and speech-in-noise perception compared to better hearing levels (Moore et al., 2020). Statistical models showed that 15 dB HL is an objectively appropriate criterion for diagnosis of significant hearing loss.

Mild and high frequency hearing loss that is missed with standard screening can be detected using newer physiologic methods such as distortion product otoacoustic emissions (DPOAE) (Blankenship et al., 2018) and auditory brainstem responses (ABR) with more sensitive criteria (Sininger et al., 2018). Our goal is to detect these milder forms of hearing loss and examine the relationship to language development in preterm infants.

Early Detection of SLD

In stark contrast to Universal Newborn Hearing Screening, there is no universal screening for speech-language risk in infants. The critical lesson from newborn screening is that intervention is more effective the sooner it can begin after birth (Joint Committee on Infant Hearing of the American Academy of et al., 2013). Because the infrastructure of newborn screening already exists for newborns in NICUs in all US states and territories, and in many other countries, employing improved screening tools before NICU discharge would be highly feasible (American Academy of Pediatrics, 2007). A greater degree of brain injury or delayed neuromaturation in language pathways, particularly in the presence of hearing loss or poorer speech processing, limits the stimulation needed to support language development. Acoustically enriched language stimulation in the first year is critical for development of normal language and later literacy skills (Nwabara et al., 2017; Vohr, 2016). Increased language exposure has been shown to be associated with increased structural connectivity, particularly in the dorsal language pathway (Romeo, Leonard, et al., 2018; Romeo, Segaran, et al., 2018). Identifying children at greater risk close to NICU discharge would allow for the provision of appropriate early intervention (i.e., increased, targeted language exposure) prior to preschool age.

Speech-language and pre-literacy deficits in premature children

Developmental testing in NICU survivors with the Bayley Scales of Infant & Toddler Development, Third Ed. is the current clinical standard for guiding early intervention in preterm infants (Anderson & Burnett, 2017). However, there is concern that this tool overestimates cognition and language and is not predictive of later impairment in preterm children (Spencer-Smith et al., 2015). Thus, in our study, we are using two specific language assessments at age 24 months: the MacArthur Child Development Inventory (MCDI) and the Communication and Symbolic Behavior Scales (CSBS). The CSBS is a direct standardized assessment particularly well-suited to the preterm population, as it assesses gestures and other non-verbal communication, allowing for a range of performance in children who are delayed in using words. We anticipate the CSBS will be sensitive to variations in communication skills not captured by the Bayley-III language subtests. At 36 months corrected age (CA), speech, language, and literacy skills are assessed using a standardized battery of speech, language, and pre-literacy tests. We are including assessment of pre-literacy skills in this population to identify precursors to later reading deficits known to occur frequently at school-age in children with a history of prematurity (Allotey et al., 2018; Borchers et al., 2019; Kovachy et al., 2015; Lee et al., 2011).

Sensitive Hearing Measures

We recently reported improved diagnosis of slight and greater hearing loss at birth by developing age-appropriate norms in well babies and preterm infants (Blankenship et al., 2018; Hunter et al., 2018). In that prospective, longitudinal study of 279 infants, hearing status was verified at 9 months CA with visual reinforcement audiometry (VRA). At approximately 1 m CA, Distortion Product Otoacoustic Emissions (OAE), Wideband Absorbance (WBA) and air- and bone-conduction diagnostic tone-burst Auditory Brainstem Responses (ABR; 0.5–4 kHz) were measured. The efficacy of DPOAE levels to classify ears as normal or hearing loss was analyzed. We found 100% sensitivity and 76% specificity for detection of slight-mild and greater hearing loss using age-specific normative algorithms, validated against the gold standard of both threshold ABR and behavioral audiometry (Blankenship et al., 2018). In that study, 10% of the preterm babies did not pass the standard newborn screening, while 30% were found to have slight or greater hearing loss. In another recent multisite study of ABR we reported that, using improved ABR techniques, we were able to detect slight or greater hearing loss (Sininger et al., 2018). We are now employing these improved techniques to precisely determine degree of all levels of hearing, assessing prevalence of hearing loss in preterm children from 3 to 36 months corrected age in a new longitudinal study of very-extremely premature children.

Methods

This preliminary report describes a longitudinal, population-based cohort study of very and extremely premature infants recruited soon after birth from five Cincinnati NICUs. These hospitals care for >90% of Southwest Ohio’s very preterm population. We have enrolled a total of 375 infants –150 infants at birth, in addition to 125 infants at 24–36 months old, who were all born at ≤32 weeks gestational age. Infants with known chromosomal or congenital conditions affecting the central nervous system were excluded, because outcomes are uniformly poor in such cases. We also excluded infants that were too medically unstable to have MRI scanning at term-equivalent age. Due to the language outcome measures, families who did not primarily speak English were excluded. We collected perinatal clinical variables known or suspected to be associated with brain injury, abnormal development, or cognitive deficits (Achenbach et al., 1993; Bapat et al., 2014; Dyet et al., 2006). Extensive data about the mother and infant (Parikh et al., 2013) were collected, along with conditions known to be associated with hearing loss, such as cleft palate or Down syndrome.

Auditory Measures

Comprehensive audiologic assements were completed between 1–5 months CA and at 2–3 years CA using age appropriate measures. At both ages, middle ear function was assessed with wideband absorbance and DPOAEs were used to evaluated inner ear function. At age 3 months CA, hearing levels were estimated using ABR,completed during natural sleep using insert earphones. ABR thresholds were used to categorize hearing status as normal hearing (NH; 0–15 dB eHL) or hearing loss (HL; ≥ 16 dB eHL). At ages 2–3 years CA, the audiology protocol included VRA and/or conditioned play audiometry (CPA) using earphones to obtain ear-specific speech detection and pure tone minimum response levels (MRLs). MRLs were used to categorize hearing status into normal hearing (NH;0–20 dB HL) or hearing loss (HL; ≥ 25 dB HL)

Speech-Language Outcomes

At 24–30 months CA, families complete the MacArthur Child Development Inventory (MCDI) – Words and Gestures, and Communication and Symbolic Behavior Scales (CSBS). The MCDI, a validated, standardized parent report of early language development, is widely used in studies of young children, may identify preschoolers with language impairment (Skarakis-Doyle et al., 2009) and has been used at 24 m to predict later language outcomes (Goodwin et al., 2002). The CSBS has good psychometric properties (McCathren et al., 2000) and has been shown in 2-yr-olds to predict expressive vocabulary one year later (Skarakis-Doyle et al., 2009). The CSBS is video recorded and scored by study staff trained with double scoring for 20% of assessments for inter- and intra-rater reliability using Cohen’s kappa. The parent/caregiver also completes the StimQ (home environment questionnaire), Dialog Parent Report (reading habits questionnaire) and Screen Exposure Parent Report (Horowitz-Kraus et al., 2017; Hutton et al., 2019; Hutton et al., 2018).

At 36 months CA, children’s articulation skills are assessed using the Goldman-Fristoe Test of Articulation-3. The Goldman-Fristoe-3 is sensitive to fricative/affricate production that is challenging for some infants with hearing loss (Moeller et al., 2007). Oral language skills will be assessed using the Test of Early Language Development-III (TELD), which is sensitive to language delays in preterm children (Monteiro-Luperi et al., 2016). A parent/caregiver also completes the MCDI – Words and Sentences. Pre-literacy skills are assessed using the Sound Blending, Letter-Word and Writing subtests of the Woodcock-Johnson-IV Tests of Early Cognitive and Academic Development, which assess phonological awareness and early alphabet/word knowledge and writing.

Results

In this preliminary analysis, 150 very/extremely preterm infants were assessed with MRI at fullterm corrected age. The Global Brain Abnormality Score, or Kidokoro Index was assessed from the MRI scans (Brouwer et al., 2017). This measure is a composite of four regional MRI measurements including cortical gray matter, total white matter, deep nuclear gray matter and cerebellar scores. In addition, we assessed an older preterm cohort—128 children tested at 2–3 years of age with the full audiologic test battery (average 30 months CA, range 24–42 months).

Auditory Measures

ABRs were completed in 133 preterm infants at 3 months CA (Range: 1–5 mos). Results showed a high percentage of infant ears with hearing loss (38%) with the degree of loss ranging from slight to moderatley severe in degree. Most ears had a sensorineural loss (18%) with a smaller percentage with a conductive component (12%) and 2% with an undetermined type of loss (Fig. 2). Results of the audiologic test protocol are shown in Figure 2. At ages 2–3 months, 32% had hearing loss in one or both ears; 12% were conductive, 18% were sensorineural and 2% were unclassified. At age 2–3 tears, the behavioral test protocol was highly successful when repeated results were included, resulting in ear-specific hearing levels in 88% of children (n=113 of 128), while 11 (9%) had only sound field MRLs, and 3% had no reliable responses. At ages 2–3 years, hearing was abnormal in one or both ears in 20% of cases. Bone conduction hearing and/or tympanometry showed a middle ear component in 13%, while 4% were sensorineural (normal tympanometry and/or elevated bone conduction) and 3% could not be classified. Of the apparent SNHL cases, all but one had passed newborn hearing screening.

Figure 2.

Figure 2.

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Hearing loss prevalence by type of loss at 1–5 months and 2–3 years, in a cohort of very and extremely premature children.

A high prevalence of hearing loss, including conductive and sensorineural type, was found in 2–3-year-old preterm children. Only 4 cases of apparent sensorineural loss had failed newborn hearing screening, indicating either missed or progressive hearing loss in 83% of cases. Age-appropriate OAE levels were highly predictive of hearing levels > 20 dB HL. The lower prevalence of sensorineural hearing loss at age 2–3 years may be due to different birth cohorts for the two age groups, or different hearing measurement techniques (ABR compared to behavioral).

Speech Language Outcomes

Standard scores for the TELD-III for receptive and expressive language subscales at 3 years CA were correlated with average hearing levels (1–8 kHz) for both ears combined in the 2–3 years CA children. As shown in Figure 3, a wide range of scores from severely low to above average was seen for both receptive and expressive language. The mean language scores tended to slope downward, with poorer average hearing levels. Notably, above average language scores were only found in children with excellent hearing levels (better than 20 dB HL). There were also a cluster of severely below average language scores despite excellent hearing levels, thus other factors are clearly at play in this cohort of premature children. Analysis using MRI, EEG and MMR measures is in progress, and hopefully will shed light on altered neurologic factors that are predictive of the language outcomes, using deep learning approaches for improved prediction of outcomes (He et al., 2020; Li et al., 2018).

Figure 3.

Figure 3.

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Correlations between Average Hearing Level and Language Standard Scores (Mean=100, SD=15) on the Test of Early Language Development in 3-year-old children. Hearing was measured at 2–3 years of age.

Intervention Methods

Early language environments and caregiver input play a critical role in shaping children’s linguistic, academic, and cognitive development (Cartmill et al., 2013; Kuhl, 2010). For slight to mild hearing loss, there are several viable intervention options, as outlined in Figure 4. These are organized using the mnemonic “HEAR” for easy reference. The first important concept for parents to be aware of is the need for communication within the infant’s “Hearing Bubble,” which is ideally within 3 to 4 feet. The caregiver’s speech will be most audible and clear within this range, and less affected by background noise that can affect speech perception (Leibold et al., 2016). At further distances, the loudness and clarity of speech drops, especially for high frequencies, thus affecting consonant reception. This range is best achieved during one-one activities with the baby that also provide language stimulation—book reading in particular. Infants benefit from lots of language stimulation, so caregivers can be coached to provide “play by play” talk whenever they are near the baby, talking about everything they are doing, naming while pointing to objects, and singing. Whenever possible, it is best to turn off extraneous sources of noise, especially electronic devices such as TV, radio, appliances, and machines. Although noise machines are highly popular among parents to encourage sleeping, they are potentially damaging to auditory development, because they produce meaningless extraneous noise, so should be discouraged. Stimulation therapies in the NICU such as Kangaroo Care and Mother-Infant Transaction Programs have been shown to improve cognitive outcomes in preterm infants later in childhood (Benzies et al., 2013; Puthussery et al., 2018).

Figure 4.

Figure 4.

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HEAR Recommendations: Management Options for Slight-Mild Hearing Loss that can be implemented from infancy onwards.

Enhanced speech environments that are natural and play-based with human caregivers provide important “incidental language cues” that serve to enhance children’s language development (Hart & Risley, 1980), and can even accelerate language growth in premature children with brain injury (Rowe et al., 2009). Quality and quantity of real language, rather than from electronic speech, such as cartoons or other recordings is preferable, particularly for children with hearing loss (Ambrose et al., 2014). To develop language and socialization, interaction with people is always best. The characteristic “baby talk or parentese” that most parents naturally use is universal across all languages, and supports language development through repetition, emphasis of prosodic cues, emotional connections, and support for theory of mind development(Ferjan Ramirez et al., 2020). An intervention approach known as “dialogic reading” involves training caregivers to read to their infants and children using shared storybooks to create conversations (reciprocal communication) with the baby or child. Dialogic reading is associated with attention-focused neural connectivity (Farah et al., 2019), and has positive impacts on both literacy and general language skills.

Amplification is effective for improved language outcomes in mild hearing loss (Tomblin et al., 2014), although it is rare for hearing aids to be recommended and worn regularly in such cases due to a lack of evidence in the past (McKay et al., 2008). Because it is not as clear in such cases that the infant is not hearing well, slight to mild hearing loss is more invisible than moderate to profound hearing loss. Parents may be less willing to invest the financial and time resources needed to obtain and implement hearing aids in such cases. However, the evidence is that infants with mild hearing loss can be as far behind as infants with more severe hearing loss, likely because they are not receiving intervention. Thus, it is always worthwhile to discuss hearing aids and the parents’ willingness to try them. It is important to explain that results will be subtle, and it may take time to see the benefit. An alternative approach is the use of remote microphone systems (RMSs) to reduce extraneous noise and bring the parent’s voice into the hearing bubble even when at a distance. A study using Language Environment Analysis Software (LENA) showed that with the use of RMS, children could have access to approximately 42% more words per day (Benitez-Barrera et al., 2018), and the amount of child-directed speech increases with use of RMS (Benitez-Barrera et al., 2019). In addition, caregivers reported positive perceived communication benefits of RMS, and they tended to talk more from a distance when using the RMS (Benitez-Barrera et al., 2018). Remote microphone technologies are especially beneficial once children are in daycare, preschool or elementary school, and can provide substantial benefits for children with slight-mild hearing loss.

ACKNOWLEDGMENTS

Supported by NIH/NIDCD R01DC018734 (Hunter, Vannest)

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