Abstract
The study aimed to assess the risk of hearing loss in full-term neonates with hyperbilirubinemia, examining the relationship between bilirubin levels, onset age of hyperbilirubinemia, and hearing impairment. Additionally, it investigated whether hearing loss was transient or late-onset, using a cost-effective double-screening method.
The study included 160 full-term neonates aged 0-1 month. Following completion of phototherapy for hyperbilirubinemia, all infants underwent initial screening with otoacoustic emissions (OAEs) and automated auditory brainstem responses (AABR). A second screening was administered to all infants within one month. Infants referred during the second screening, regardless of their first screening results, underwent diagnostic evaluation. For analysis, the infants were categorised into 4 groups, based on their bilirubin levels and onset of jaundice.
After the initial screening, 37% of infants were referred, which decreased to 9% after subsequent screening, suggesting transient hearing loss in 76% of initially referred infants. Permanent hearing impairment was confirmed in 2.5% of infants following diagnostic evaluation, with 3 infants diagnosed with ANSD and 1 infant with sensorineural hearing loss, all from categories characterized by elevated bilirubin levels. The findings indicated that even bilirubin levels as low as 12 to 15 mg/dl could lead to hearing loss, particularly when jaundice onset occurred early.
This study highlights the effectiveness of double-screening for identifying transient hearing losses in infants with hyperbilirubinemia, minimizing the need for diagnostic referrals. It underscores the importance of considering both bilirubin levels and onset timing to assess auditory risk fully.
Keywords: Hearing screening, Hyperbilirubinemia, Neonates, Bilirubin levels, Age of onset, Double, Stage screening
Hyperbilirubinemia is prevalent among newborns, affecting 60% of full-term and 80% of preterm infants [1]. Research links neonatal hyperbilirubinemia with high rates of hearing loss, up to 20–22% [2]. Early intervention is crucial to support language and speech development in affected infants, prompting global implementation of newborn hearing screening programs [3].
Though medical authorities have established strict guidelines for promptly identifying and treating neonatal jaundice, hyperbilirubinemia can develop between the 1st and 8th day after birth, even post-hospital discharge [4, 5]. Infants who develop jaundice after initial hearing screening or discharge are at increased risk of hearing loss, potentially unnoticed if they have already passed screening. Thus, rescreening infants’ auditory status after jaundice episodes is necessary, regardless of previous screening outcomes [6].
Numerous studies have explored the link between jaundice and hearing loss in newborns. Some researchers have observed a correlation between total serum bilirubin levels and hearing impairment [7–9]. For example, one study noted that 33% of newborns with blood bilirubin levels ranging from 15 to 25 mg/dL showed affected wave complexes IV and V in ABR tests [10]. In another study involving 200 newborns with serum bilirubin levels over 20 mg/dL, Boskabadi et al. [8] found that 4.8% of these infants had sensorineural hearing loss, suggesting that severe jaundice may increase the risk of hearing loss by 10 to 50 times. However, conflicting findings exist in the literature, with studies reporting no significant association between neonatal hyperbilirubinemia and hearing impairment [2, 11].
Despite extensive research on the link between bilirubin levels and hearing loss, there’s a lack of studies on when elevated bilirubin levels appear and their combined impact on hearing. Boo et al. [2] explored risk factors for jaundice-induced hearing loss and found no direct link between total bilirubin levels and hearing impairment. Instead, they noted a correlation between exchange transfusion and the age when jaundice begins. Thus, it’s crucial to consider both jaundice onset age and bilirubin levels when studying their association with hearing loss [12]. This holistic approach will improve understanding of the critical period when high bilirubin levels might risk hearing impairment.
Moreover, some studies suggest hearing loss in jaundiced infants may improve over time [11, 13, 14], underscoring the need for regular testing. This is challenging in densely populated countries like India due to limited infrastructure for diagnostic referrals. Hence, reassessment screenings are vital, possibly starting one month after treatment, to track recovery and assess hearing status during this critical early phase.
The main objective of this study was to estimate the risk of hearing loss among term neonates affected by hyperbilirubinemia while also examining the correlation between bilirubin levels, the age of onset of hyperbilirubinemia, and hearing loss. Additionally, the study aimed to investigate whether hearing impairment in these infants was temporary or late-onset, utilizing an economical test-retest double-screening method.
Methods
The study was carried out following the guidelines of the institutional review board, and ethical approval was obtained (DOR.9.1/PhD/MMB/PR19/2021-22).
Participants
The study enrolled a cohort of 160 full-term neonates. Inclusion criteria encompassed infants aged 0 to 1 month, born at early term and full term [15], with average birth weight [16], who were admitted for phototherapy for a minimum of 12 h within the first two weeks after birth, regardless of their bilirubin levels. Exclusion criteria comprised neonates with any other risk factors for hearing loss as outlined by Joint Committee of Infant Hearing (JCIH) 2009, as well as those who failed a hearing screening test before the onset of jaundice.
Procedure
In this cross-sectional study, all neonates underwent hearing screening soon after completing treatment for hyperbilirubinemia, when Total Serum Bilirubin (TSB) levels normalized. Screening employed an initial otoacoustic emissions (OAEs) and automated auditory brainstem responses (AABR) and results were noted. Subsequently, all neonates underwent a second screening with OAEs and AABR within one month. Infants who passed the second screening were discharged, while those who did not were referred for diagnostic audiological evaluation.
Distortion product OAEs (DPOAEs) were recorded using the ERO•SCAN device (MAICO Diagnostics, Berlin) from participants’ ears. Stimuli were presented at 65/55 dB SPL for frequencies 2, 3, 4, and 5 kHz. The pass criterion required a signal-to-noise ratio (SNR) of at least 3 dB across three consecutive frequency bands out of four (2 kHz, 3 kHz, 4 kHz, and 5 kHz) [17]. AABR was conducted using the ‘Easy Screen’ BERA phone (MAICO Diagnostics, Berlin). Click stimuli at 35 dB nHL were presented ipsilaterally at a rate of 11.1/sec. Electrodes were placed with the positive on the forehead, negative on the test ear mastoid, and ground on the tragus area of the test side. Pass or refer status was automatically determined.
Infants referred from the second screening stage underwent diagnostic ABR using the VivosonicTM Integrity ABR System (Toronto, ON, Canada). Clicks with alternating polarity were used to record ABR at a rate of 11.1/s. A vertical montage with a 30 –3000 Hz filter and 2000 sweeps were employed. Infants diagnosed with hearing loss were referred for further rehabilitation. Figure 1 outlines the study’s methodological flow.
Fig. 1.
Flow chart outlining the research procedure
Data Analyses
All session results were recorded in Statistical Package for Social Sciences version (SPSS 26, IBM, Chicago, USA) for analysis. Pass and refer outcomes were coded as “1” for pass and “0” for refer. Neonates were grouped based on bilirubin levels and jaundice onset timing into four categories: early high (TSB ≥ 15 mg/dl within 72 h), early low (TSB <15 mg/dl within 72 h), late high (TSB ≥ 20 mg/dl after 72 h), and late low (TSB <20 mg/dl after 72 h). This categorization was done following the framework outlined in the study by Porter et al. [18].
Results
The infants were categorized into four groups (G1: early high, G2: early low, G3: late high, and G4: late low) based on their bilirubin levels and the timing of jaundice onset. There were 67 infants in the first category, 32 in the second category, 20 in the third category, and 41 in the fourth category, totalling 160 infants. The summary of the groups with TSB level, timing of jaundice onset, and number of participants in each group is provided in Table 1.
Table 1.
The summary of the groups with TSB level, timing of jaundice onset, and number of participants in each group
| Groups | TSB level | Timing of jaundice onset | Number of infants |
|---|---|---|---|
| G1-Early High | ≥ 15 mg/dl | within 72 h of birth | 67 |
| G2-Early Low | <15 mg/dl | within 72 h of birth | 32 |
| G3-Late High | ≥ 20 mg/dl | after 72 h of birth | 20 |
| G4-Late Low | <20 mg/dl | after 72 h of birth | 41 |
Results of First-Stage Hearing Screening
The initial hearing screening results, which included OAEs and AABR for all the neonates, are presented in Table 2.
Table 2.
Pass and refer results of AABR and OAEs during the first stage screening
| AABR Pass | AABR Refer | Total | |
|---|---|---|---|
| OAE Pass | 99 | 40 | 139 |
| OAE Refer | 2 | 19 | 21 |
| Total | 101 | 59 | 160 |
Table 1 reveals that 40 neonates exhibited OAEs present and AABR absent, which may suggest Auditory neuropathy spectrum disorder (ANSD) [6]. Additionally, 21 neonates did not pass the OAEs, and Fig. 2 depicts the distribution of these neonates across groups in the two stages of screening. Furthermore, 59 infants did not pass the AABR screening, with Fig. 3 illustrating the distribution of these results across the predominant hyperbilirubinemia groups.
Fig. 2.
Distribution of OAE referrals across categories after the first and second screening stage
Figure 3.
Distribution of AABR referrals across categories after the first and second screening stage
The figure illustrates the outcomes of infants following OAE screening, indicating “G” for the initial screening and “G*” for the second screening.
The figure illustrates the outcomes of infants following AABR screening, indicating “G” for the initial screening and “G*” for the second screening.
The findings indicate that 13% of infants were referred in OAE screening and 36.9% in AABR during the first screening. Among the infants referred to in OAE, 4.3% belonged to the first category, 2.5% to the second category, 3.1% to the third category, and 3.1% to the fourth category. A chi-square analysis showed no significant difference in referral rate across groups. AABR referrals showed that 18.1% were referred from the first category, 3.8% from the second category, 8.8% from the third category, and 6.3% from the fourth category. Further, a chi-square analysis indicated a significantly greater number of referred cases in category 3 compared to other categories, with category 1 being the next most prominent. Table 3 provides the chi-square values obtained for AABR screening for comparison between groups.
Table 3.
The chi-square results to compare the AABR referrals for hearing loss between groups
| Categories compared | Chi-square value, Degrees of freedom, Significance |
|---|---|
| Category 1 and 2 | (χ2 = 5.70; df = 1; p = 0.017)* |
| Category 1 and 3 | (χ2 = 4.39; df = 1; p = 0.036)* |
| Category 1 and 4 | (χ2 = 3.93; df = 1; p = 0.043)* |
| Category 2 and 3 | (χ2 = 13.65; df = 1; p = 0.000)* |
| Category 2 and 4 | (χ2 = 0.33; df = 1; p = 0.56) |
| Category 3 and 4 | (χ2 = 11.71; df = 1; p = 0.001)* |
Results of Second-Stage Hearing Screening
The results of the second-stage screening, including OAE and AABR for all the infants, are presented in Table 4.
Table 4.
Pass and refer results of AABR and OAE during the second stage screening
| AABR Pass | AABR Refer | Total | |
|---|---|---|---|
| OAE Pass | 145 | 9 | 154 |
| OAE Refer | 0 | 6 | 6 |
| Total | 145 | 15 | 160 |
It can be noted that, in the first stage of screening, 40 infants showed signs of ANSD. However, by the second screening stage, these infants had improved in their auditory condition, leaving only nine infants exhibiting symptoms of ANSD. Among the 19 infants who did not pass both screening tests initially, only five failed both tests during the second screening, while the remaining infants passed. One infant who had passed the initial screening was referred in both OAE and AABR in the second screening. 15 infants referred through the second AABR screening were further referred for diagnostic evaluation.
Figure 3 displays the distribution of infants referred across hyperbilirubinemia categories.
The findings revealed that 9.3% of neonates did not pass the second-stage screening. Among them, 3.8% of referrals were from the first category, 1.25% belonged to the second category, 3.8% were in the third category, and 0.6% fell into the fourth category.
The chi-square test was not conducted to compare the referrals between categories due to the limited numbers observed in certain cells. Table 5 displays infants’ referral and pass data from both screening sessions.
Table 5.
Pass and refer results based on AABR after two hearing screening sessions
| Pass (2nd Screening) | Refer (2nd Screening) | Total | |
|---|---|---|---|
| Pass (1st Screening) | 99 | 1 | 100 |
| Refer (1st Screening) | 46 | 14 | 60 |
| Total | 145 | 15 | 160 |
Notably, 46 infants showed improvement during the second screening, whereas one infant was referred during the second screening despite passing the first one.
Results of Diagnostic ABR Evaluation
Table 5 shows that 15 infants were referred in the second screening. Among them, 9 infants exhibited signs of ANSD, with AABR referral and OAE pass. Diagnostic results for these 9 infants indicated 3 with ANSD, 3 with normal ABR indicating typical hearing sensitivity, and 3 lost to follow-up. Additionally, among the 6 infants referred for both OAE and AABR, results showed 3 with conductive hearing loss, 1 with sensorineural hearing loss, 1 with normal ABR, and 1 lost to follow-up. Analysis of infants with sensorineural hearing loss revealed 2 in the first category and 2 in the third category. Table 6 outlines the distribution of hearing statuses among infants referred for diagnostic assessment.
Table 6.
Distribution of hearing status of infants after diagnostic evaluation
| Hearing Status | Frequency | Severity |
|---|---|---|
| Sensorineural hearing loss | 1 (late onset) | Profound |
| ANSD | 3 | ANSD |
| Conductive hearing loss | 3 | 2 mild to moderate and 1 mild |
| Normal hearing sensitivity | 4 | NA |
| Lost to follow up | 4 | NA |
Discussion
In this study, 37% of infants were referred after initial AABR screening. Similarly, high referral rates (56.7%) were noted in infants with hyperbilirubinemia [9]. Initial OAE screening showed a 13% referral rate. Interestingly, among infants passing OAEs, 40 failed AABR, indicating possible ANSD symptoms. This aligns with Boo et al.‘s findings [7] where 37 of 44 infants with SNHL had normal OAE responses. Hyperbilirubinemia is identified as a significant factor contributing to ANSD, potentially damaging auditory pathway neurons [6, 19]. Uss K. [20] supported these findings, suggesting a retro-cochlear lesion site affecting neural but not OAE responses in most infants.
After initial screening, the study observed high referral rates in Category 3 (late high, 70% referred) and Category 1 (early high, 43% referred), consistent with prior studies noting elevated referrals in high bilirubin levels [8]. Our findings suggest bilirubin levels as low as 12 to 15 mg/dl shortly after birth pose significant auditory risk. Referrals also occurred in Category 2 (early low, 19% referred) and Category 4 (late low, 24% referred), indicating potential auditory disorders, consistent with findings of hearing loss irrespective of bilirubin levels [21, 22].
Despite extensive research on hyperbilirubinemia’s impact on hearing loss, there’s a paucity of follow-up studies evaluating infants’ hearing status shortly after initial screening, such as within a month. Post-second screening, referrals notably dropped from 37 to 9%, suggesting transient hearing loss in 76% of initially referred infants. Recovery rates varied: 34% in Category 1, 15% in Category 2, 40% in Category 3, and 22% in Category 4. Improved auditory status has been observed in infants referred for hyperbilirubinemia-related hearing loss [23]. Chen et al. [6] reported similar findings, identifying 13 infants with ANSD and 27 with SNHL during diagnostic follow-up. Among the 13 with ANSD, 7 showed resolved hearing loss, and 3 improved; the 27 with SNHL outcomes were not detailed. They noted hearing improvement in infants with bilirubin levels below 408.6 ± 129.0 µmol/L but did not consider jaundice onset age. Nickisch et al. [19] suggested that transient hearing loss in some infants may stem from neurotoxic effects dissipating over time.
Our study identified confirmed permanent hearing loss in four infants, resulting in an incidence rate of 2.5% among infants with hyperbilirubinemia after undergoing two rounds of screening and diagnostic evaluation. This incidence appears lower compared to findings from the literature [20, 24, 25], likely attributed to our approach of double screening and delayed diagnostic evaluation. This allowed for identifying infants with recovered auditory status and thus filtered out some cases from the final count.
During the screening and diagnostic processes, it became evident that infants showed high referrals in categories 3 and 1, along with unresolved hearing loss following diagnostic assessments. Two infants in category 1, both with hearing loss, had TSB levels of 15.2 mg/dl on the first day and 15.5 mg/dl on the second day. In category 3, two infants recorded TSB levels of 25 mg/dl on the fourth day and 34 mg/dl on the fifth day. This suggests that elevated bilirubin levels may contribute to increased referrals, with even levels as low as 15 mg/dl in the initial days after birth posing a significant risk for hearing impairment. This contradicts studies that assert a direct correlation between total serum bilirubin levels and hearing loss without considering the timing of bilirubin peak levels.
Another significant study finding is that infants with lower bilirubin levels (Category 2 and 4) exhibited auditory dysfunction during the initial screening, which resolved in all infants within two months. This outcome is consistent with the findings of Chen et al. [6], who observed the recovery of auditory function in most infants with bilirubin levels within the range of 408.6 ± 129.0 µmol/dl (approximately 23.91 ± 7.56 mg/dL) within 12 months. Similarly, Gupta and Mann [22] reported a recovery rate of 33.33% in infants with a mean bilirubin level of 19.46 mg/dL, and an 80% recovery rate in infants with a mean serum bilirubin level of 15.97 mg/dL after a retest conducted one month later. However, our study underscores the importance of considering both bilirubin levels and the timing of onset, suggesting that low bilirubin levels in the later days after birth pose a shallow risk of hearing loss.
Our research identified an infant who developed late-onset hearing loss who initially passed both OAE and AABR screenings but failed the subsequent screening and was diagnosed with bilateral profound hearing loss. This raises concerns about the efficacy of one-time screening models, potentially overlooking late-onset hearing loss in infants with hyperbilirubinemia.
Conclusion
This study offers valuable insights into cost-effective rescreening strategies that could be implemented in developing countries to monitor the development of hearing loss in infants with jaundice. By conducting diagnostic tests only after two rounds of screening using OAE and AABR, the need for diagnostic appointments is minimized, facilitating the identification of infants with transient hearing losses, common among infants with jaundice, thereby streamlining the diagnostic process. The statistical insights provided by this study regarding transient hearing loss in infants with neonatal jaundice can be pivotal in counseling parents and alleviating parental anxiety. Furthermore, the study highlights the potential for late-onset hearing loss in these infants. It emphasizes the importance of considering the timing of jaundice onset and TSB levels to understand the extent of auditory toxicity fully.
Funding
All India Institute of Speech and Hearing has no such involvement.
Declarations
Conflict of Interest
Authors declare no conflict of interest.
Informed Consent
Written informed consent was taken from the guardians of all the participants for their willingness to participate in the study.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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