Universal newborn hearing screening (UNHS) programs are early hearing detection and intervention programs aimed at the early identification, habilitation, and follow-up of children with congenital permanent hearing loss (Anon 2019). Such programs are considered of paramount importance for the prevention of developmental delays (Yoshinaga-Itano et al. 2018). During the last year, coronavirus disease 2019 (COVID-19) pandemic has profoundly changed many aspects of our profession as otolaryngologists (Parilli-Troconis et al. 2020), and hospitals have been plagued by organizational issues determined by lack of personnel, internal outbreaks, and diversion of human and economic resources to COVID wards and COVID intensive care units. At our institution (Azienda Ospedaliero Universitaria di Sassari), all services, including essential ones, have been impacted, especially at the height of the crisis. Even if our screening service was closed for only 3 weeks during March 2020 due to a COVID outbreak inside the hospital, and patients involved were readily rescheduled, we deemed anyway an appropriate analysis of the impact of the pandemic on our screening program as mandatory, to plan for eventual corrective measures. Our hypothesis was that COVID-19 potentially could still have had an impact on our screening program both in a direct manner, behaving like a risk factor, and indirect manner, by keeping the parents from coming back for retests due to fear of being exposed to infection, or due to the restrictive policies both at an institutional and at a national level concerning the access to our hospital (mask mandates, temperature screening, need for a recent nasal swab). Early reports describing a potential impact of COVID-19 on the auditory system of adults (Mustafa 2020), newborns’ medial olivocochlear efferent system (Celik et al. 2021), and on screening results (Alan & Alan 2021; Oskovi-Kaplan et al. 2021), further motivated us to explore its potential role as a risk factor in our screened population.
MATERIALS AND METHODS
The present study was aimed at assessing the impact of COVID-19 pandemic on the UNHS of Azienda Ospedaliero Universitaria di Sassari (active since 2012) and the potential role of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) as an audiological risk factor. Our Institution is a second-level facility and a referral center for six other hospitals located in Northern Sardinia and provides a UNHS service and all the equipment and personnel necessary to offer a final diagnosis and appropriate therapy on-site. According to the Italian National Institute of Statistics (2020), the served area has a population of 330.211 individuals and a birth rate of 5.8‰. All newborns at our institution are screened with transient evoked otoacoustic emissions (TEOAEs) before discharge (within 3 days). Newborns referred from other hospitals are usually screened within the first week of life as outpatients. A team of experienced audiology technicians performs the tests in a noiseless setting. Newborns with a bilateral or unilateral “refer” result are referred to the second stage, which involves a retest with TEOAEs planned within 30 days of life, and parents are required to come back to our facility. Neonatal intensive care unit (NICU) newborns not already discharged are tested again as inpatients. Parents of babies referred to retest are counseled, to manage parents’ anxiety and minimize the rate of lost to follow-up, and the parents are called at least once to book a new appointment if they fail to show up with the newborn to the second stage. During 2020, the team, the instrumentation, and our protocol were kept unchanged. To test our hypothesis, we selected as main outcomes of the study the time to retest (days passed between the first and second stage TEOAEs), the loss to follow-up rate (no show at second level TEOAEs), and the referral rate among newborns born to SARS-CoV-2 polymerase chain reaction (PCR) positive mothers during 2020. Two groups were selected, all newborns tested at our facility during 2020 (group 1) to represent a sample of newborns potentially affected by the pandemic, and all newborns tested during 2019 (group 2) to represent a homogenous and comparable subset of newborns not affected by the pandemic. The rate of refer at the first stage of newborns born to SARS-CoV-2 PCR positive mothers during 2020 was compared to the rate of refer at the first stage of all the wellborn newborns born to SARS-CoV-2 PCR negative mothers during the same year. Data were retrieved retrospectively from our electronic database. Statistical analysis was performed with JASP (JASP Statistics, Version 0.16.3, University of Amsterdam). Time to retests for the two groups was compared using a Mann-Whitney U test. Lost to follow-up among group 1 and group 2 newborns were compared with Pearson’s Chi-square test. Statistical tests were considered significant for p ≤ 0.05.
A total of 1555 newborns in 2019 (439 NICU and 1116 non-NICU) and 1346 newborns in 2020 (344 NICU and 1002 non-NICU) were screened by our service. Time to retest comparison along with inherent descriptive statistics is shown in Table 1. Loss to follow-up by group and Pearson’s Chi-square test results are shown in Table 2. Among SARS-CoV-2 PCR positive mothers’ newborns, only one was referred to the second stage of screening (1/21; 4.76%), a higher percentage was seen among newborns born to SARS-CoV-2 PCR negative mothers 69 of 960 (7.19%). The only referred newborn in the COVID group, passed the second stage of screening, and had a normal auditory threshold at the diagnostic auditory brain stem response, offered to the parents not as part of our screening protocol but as a precautionary diagnostic examination.
TABLE 1. -
Time to retest (days) comparison (group 1 vs. group 2), results of descriptive statistics and Mann-Whitney U test are shown.
|Set of patients
||Mean time to retest (days)
| Group 2
| Group 1
| Group 2
| Group 1
| Group 2
| Group 1
NICU, neonatal intensive care unit.
TABLE 2. -
Loss to follow-up (after stage I) by year and results of Pearson’s Chi-square test for contingency tables
|Set of patients
p (OR; IC)
||0.065 (–0.747; –1.549 to 0.056)
||0.826 (–0.318; –3.164 to 2.527)
||0.074 (–0.688; –1.454 to 0.078)
NICU, neonatal intensive care unit; IC, confidence interval; OR, odds ratio.
Contrary to our initial assumption, our screening program, at least in relation to the outcomes explored and within the limits of the present study, has not been significantly affected by COVID-19. In particular, we were afraid that, due to the limitations and rules imposed to access the hospital, and parents’ fear of coming back to the hospital, less newborns were coming back for the second stage and at a later time than indicated, impeding a timely early diagnosis (Yoshinaga-Itano 2004). Both the comparison of time to retest and loss to follow-up seem to confirm that there is no meaningful difference between group 1 and group 2. While a potential effect of parental anxiety due to COVID-19 on the number of lost to follow-up has been already hypothesized (Alan & Alan 2021), we were not able to find any published data on the matter. Our data highlight a higher time to rest for newborns coming from the NICU, significantly out of the recommended 1 month timeline (Anon 2019). While we are usually able to meet the 1-3-6 timeline with wellborn infants, we have more difficulties with NICU newborns mainly due to clinical factors (medical priorities that sometimes delay the retest).
A potential tropism of SARS-CoV-2 for the auditory system and a possible resulting damage have been reported in the literature with contrasting results (Mustafa 2020; Almufarrij & Munro 2021; De Luca et al. 2021; Gallus et al. 2021). A recent study conducted on newborns exposed to the virus during pregnancy that passed the screening auditory brain stem response, hypothesized that SARS-CoV-2 might cause an insufficiency of the medial olivocochlear efferent system (Celik et al. 2021). Alan & Alan (2021) reported in a recent article that in their series of 118 infants born to mothers with SARS-CoV-2 PCR positivity during pregnancy a significantly higher rate of refer results at the first stage of screening was observed in comparison to a homogeneous control group. They also found that neonates whose mothers had positive PCR results in the second trimester were more likely to have refer results. However, any difference disappeared by the second stage (Alan & Alan 2021). A more recent article by Oskovi-Kaplan et al (2021) reported on 458 newborns born to mothers with SARS-CoV-2 PCR positivity during pregnancy. In their series, 12.4% in the COVID-19 group and 9.4% in the control group failed their first stage of screening, while 1.3% of the COVID-19 group and 2.9% of the control group failed the second stage of screening. The reported differences did not reach statistical significance. They also grouped the newborns according to the trimester when the mother had COVID-19, finding that the group of the second and third trimester had higher rates of failure at the first stage of screening, but that difference was absent at the final testing. In our series, the rate of refer results among newborns born to SARS-CoV-2 positive mothers at first stage was comparable to the control group, and this confirms that COVID does not seem to behave as a relevant congenital audiological risk factor.
The present study has several limitations. Time frame selection for group 1 is debatable. We settled with the beginning of 2020 as the first wave in Italy was relatively early and by that time, the information and warnings about COVID were already strong (hence parental anxiety). We compared this group only to 2019, a choice dictated by the willingness to have uniform groups in terms of numbers, but also of setting, protocols and personnel involved. Moreother, a possible impact of COVID-19 could have emerged by an analysis of the number of newborns referred to our hospital by other centers or by the efficiency of our program in terms of time needed to test in a COVID setting and related costs but that was either nonpractical or impossible to assess with the available data. Due to the relatively small number of newborns from mothers with a SARS-CoV-2 infection during pregnancy, the significance of the results on the matter is limited, and more studies will be needed to definitely exclude a role of SARS-CoV-2 as an audiological risk factor, especially in relation to different phases of pregnancy as done in other reports (Alan & Alan 2021; Oskovi-Kaplan et al. 2021).
Right now, while we progressively shift to a more stable, predictable and cyclic phase of the pandemic, we are faced with the challenge of “normalizing” the current situation and adopting all the needed corrections to our workflow. Staff shortages in our country are becoming less severe thanks to the introduction of new policies that include the elimination of the isolation period in case of “close contact” with a COVID-19 patient, the reduction of the isolation period for SARS-CoV-2 infection for full vaccinated patients (including the medical personnel), and an easier access for personnel from other medical structures if support is needed, as many hospitals in our region are no more burdened by dedicated COVID wards. Moreover, patients can now easily access the hospitals as the need for a vaccination certificate or a recent nasal swab (“Green Pass”) is no longer mandatory. We are also enacting a proactive recall policy to be sure that all of our newborns come back for their retest despite potential difficulties (as SARS-CoV-2 positive parents). We believe that each hospital with a UNHS program should plan a similar recall policy and perform a periodical audit of their screening program to find any flaws in that sense. We believe that this phase, free of the constraints of a constant emergency state, harbors the potential to allow for further well-planned research, both on the effects of SARS-CoV-2 on the auditory system, and on policies that will allow essential services as the UNHS up and running even during difficult times.
All authors contributed equally to this work. L.M.D.L. and R.G. wrote the main paper and participated in data collection; A.M., S.P., E.D. and D.R. participated in data collection; R.G. and F.B. revised the final manuscript, helped with data interpretation; R.G., F.B. and D.R. revised the final manuscript, performed data analysis and data interpretation; A.P. assisted with the revision process and statistics of the revised paper. All authors discussed the results and implications and commented on the manuscript at all stages.
We thank Maria Lucia Piras, Francesca Arca Sedda and Giovanna Maria Canu for their invaluable help with data collection.
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