Abstract
Introduction
Gestational diabetes is a potential risk factor for neonatal hearing loss. Increased circulating sugars in mothers during pregnancy can impairs the micro circulation and can cause congenital anomalies of the inner ear resulting in congenital hearing loss. This study attempts to find the incidence of neonatal hearing loss among diabetic mothers.
Methodology
This was a case control study with 86 neonates of diabetic mothers as cases and neonates of non diabetic mothers(n = 86) as controls. Antenatal diabetic history and sugar values of mothers were documented. Hearing status of the neonates were tested using DPOAE test and ABR test. DPOAE test was done on 3rd day and those who did not get a positive response underwent 2nd DPOAE and also ABR test if 2nd DPOAE was negative.
Results
All neonates underwent DPOAE test and few were lost on follow up. First and second DPOAE showed a statistically significant difference between cases and controls. All babies who underwent ABR test had abnormal waveforms. 98% of cases showed moderate and severe bilateral hearing loss whereas all controls had only mild bilateral hearing loss.
Discussion
This study showed a significantly higher percentage of abnormal hearing outcome among neonates of diabetic mothers than non diabetic mothers. This could be because of the toxic effects of maternal hyperglycemia on developing auditory system of the fetus. This study emphasis the need for better glycaemic control in diabetic pregnancy, the importance of early and mandatory hearing screening in newborns of diabetic mothers.
Keywords: Neonatal Hearing loss, Neonatal Hearing Screening, Gestational Diabetes Mellitus, DPOAE, Auditory Brain stem Response
Introduction
Hearing sense helps individuals to get connected with their surroundings. Every 2 to 4 neonates in 1000 birth are born with hearing loss [1]. This can consequently delay the speech development and language abilities of the child [2]. There are multiple maternal, metabolic diseases which can result in neonatal hearing loss including gestational diabetes mellites The purpose of this study is to find the incidence of hearing impairment in neonates of diabetes mother using audiological tests like Distortion Product otoacoustic Emission (DPOAE) and Auditory Brainstem Response (ABR). Early hearing screening is mandatory in neonates of diabetic pregnancy to prevent the hearing disability.
Materials and Methodology
This was a prospective study done in a tertiary care hospital over a period of 18 months. This study was conducted after approval from the Institutional Ethics Committee under the tenets of Declaration of Helsinki as per National Ethical Guidelines for Biomedical Research involving human participants of the Indian Council of medical research (ICMR),2017.
This was an observational case control study, consisting of 172 newborn babies, including 86 newborns of diabetic mothers and 86 newborns of nondiabetic mothers, which was done for a period of one year from Jan 2021 to march 2022. The study was conducted after getting written informed consent from all parents. Antenatal history including the diabetic history were taken retrospectively. Blood sugar values of diabetic mothers during pregnancy were documented. All newborns were evaluated with screening DPOAE test.
(Intelligent Hearing System, IHS, Florida, USA) on the third day of birth. The results were interpreted as PASS (normal ) or REFER. Those who got the normal DPOAE response were taken as DPOAE PASS and those who did not get a response were taken as DPOAE REFER.The neonates who failed in this initial test were subjected for repeat DPOAE test after 45 days. Those who failed in second DPOAE test, were evaluated using ABR test (Neuroaudio neurosoft Ivanavo,Russia) after one month. In this study we compared the incidence of hearing loss among neonates of diabetic and non diabetic mothers as well as incidence of hearing loss among Gestational and Overt Diabetes Mellitus mothers.
Statistical Analysis
Statistical analysis for the data was done by Chi-square test, and Independent sample t test was applied to compare the quantitative variables between the groups( cases and control). The data was analyzed using SPSS(version 20). The p Value < 0.05 was considered as significant.
Results
A total of 172 newborns (86 cases and 86 controls) who satisfied the inclusion criteria were studied for a period of one year. There were 86 newborns of diabetic mothers as cases and same number of newborns of non diabetic mothers as controls. Among this 84 ( 48.8%) were female babies (cases = 43 females, controls = 41 females )and 88 (51.2%) were male babies (cases = 43, controls = 45). On comparing the mean birth weight among cases and controls, case group had a relatively higher mean birth weight (2.82 +/0.40 kg) when compared to controls (2.75 +/0.49 kg). However the difference was not statistically significant (p Value- 0.26).
Mean random sugar values on the first day of birth, for the case group was 61.10 mg/dl (maximum sugar value was 86 mg/dl and a minimum sugar value of 42 mg /dl) and for control group, it was 73.80 mg/dl(maximum − 98 mg/dl and minimum 48 mg/dl). It was observed that the neonates of diabetic mothers had a lower mean sugar value as compared to controls and the difference in the value was found to be statistically significant (P value 0.001).
The case group had a relatively higher APGAR score at 1 and 5 min than the controls at the same time. The cases showed a mean APGAR score of 7.44+/-0.745 at 1 min and 9.51 +/-0.628 at 5 min, and the controls showed a score of 6.97 +/-1.121 at 1 min and 9.02+/-0.958 at 5 min .
On first DPOAE test, among the 86 cases, 21newborns (24.4%) showed REFER status on the right ear and 52 (60.5%) showed REFER on left ear whereas 18 babies had REFER status on both ears. Among the case group, 55 newborns out of 86 had REFER status. Whereas among controls 8 babies(9.3%) showed REFER on right side and 32 babies (37.2%) had REFER on left side and 2 neonates showed bilateral REFER status (Chart 1). The study showed the newborns of diabetic mother had significant abnormal hearing screening outcome on both ears compared to the controls .We also observed more number of PASS status in both ears for control groups. The difference in REFER status for each side among case and control group was statistically significant with p Value of 0.008 on right ear and 0.002 on left ear.
Chart 1.
Distribution of subjects based on first OAE results
On second OAE, 53 cases and 34 controls were evaluated after excluding the subjects who got PASS status in first test and those who lost follow up (2 cases and 4 controls didn’t turn up for second OAE evaluation). Among the cases, 21 babies(38.2%) had REFER status on right ear, 39 babies (70.9%) on left ear and 17 babies had bilateral REFER status. Among controls, 4 babies(10.5%) showed REFER status on right ear, and 16 babies REFER status on left (42.1%) ear and 1 baby showed refer status on both ear. (Chart 2). It was observed that neonates of diabetic mothers had more REFER status than the neonates of non diabetic mothers which was statistically significant with a p Value of 0.009 and 0.019 on right and left ear respectively.
Chart 2.
: Distribution of subjects based on 2nd OAE results
Among cases, 43 babies and 19 babies among controls had REFER status on second OAE and they were called for ABR after one month. There were 33 cases and 5 controls for ABR test, after excluding those who did not turn up for follow ups (10 cases and 14 controls had lost follow up). All cases and controls who underwent test showed abnormal waveforms. The ABR test results showed a statistically significant difference (p = 0.001) among case and control group with more number of case group subjects had abnormal ABR waves (p = 0.001).
The ABR test results for the case group were Bilateral 5th peak absent at 90 db for 16 babies which comes under severe hearing loss, Bilateral 5th peak present till 70 db for 15 babies which comes under moderate hearing loss, and Right 5th peak present till 70 db for 2 babies which comes under Unilateral right sided moderate hearing loss ,based on Goodman’s classification.7 All the 5 controls had bilateral 5th peak present till 50 db which is classified as mild hearing loss depicted in Table 1.
Table 1.
Distribution of subjects based on ABR results
| ABR | Groups | Total | ||
|---|---|---|---|---|
| Cases | Controls | |||
| Severe HL | Count | 16 | 0 | 16 |
| % | 48.48% | 0.0% | 42.10 | |
| Bilateral moderate HL | Count | 15 | 0 | 15 |
| % | 45.45% | 0.0% | 39.47% | |
| ModerateHL-Unilateral(Right ear) | Count | 2 | 0 | 2 |
| 6.06% | 0.0% | 5.26% | ||
| Mild HL- bilateral | Count | 0 | 5 | 5 |
| % | 0.0% | 100% | 13.15% | |
| Total | Count | 33 | 5 | 38 |
| % | 100.0% | 100.0% | 100.0% | |
Chi-square value- 38, p value- 0.001*
Among the 86 cases, 80 were newborns of GDM mothers and 6 were newborns of Overt Diabetes mother. Among the GDM ,14 neonates had severe hearing loss, 13 neonates with bilateral moderate hearing loss, 2 neonates with unilateral moderate hearing loss based on ABR results. In overt diabetes, Among 6 babies of overt diabetic mothers, (67%) 2 babies had severe hearing loss and another 2 had bilateral moderate hearing loss. There was no statically significant difference in hearing outcome among these 2 groups in this study ( p Value 0.78) (Table − 2.
Table 2.
ABR results of neonates of GDM mothers with Overt DM mothers
| Cases (neonates) |
ABR results | Total | ||
|---|---|---|---|---|
| Severe HL | B/L moderate HL | U/L moderate HL(Right) | ||
| GDM | 14 | 13 | 2 | 29 |
| 42.42% | 39.39% | 6.06% | 87.87% | |
| Overt DM | 2 | 2 | 0 | 4 |
| 6.06% | 6.06% | 0.00% | 12.12% | |
| Total | 16 | 15 | 2 | 33 |
| 48.48% | 45.45% | 6.06% | 100.00% | |
We have grouped the mothers based on their antenatal HbA1C in the first trimester into 4 groups, Group 1 consisting of mothers with HbA1C of 6, Group 2 consisting of mothers with HbA1C values between 6 to 6.5, Group 3 consisting of mothers with HbA1C values 6.6 to 7 and Group 4 consisting of mothers with HBA1C values more than 7. The frequency of mothers were 20 (23.3%), 24 (27.9%), 24 (27.9%) and 18 ( 20.9%) respectively in each groups. The majority of mothers (56%) belonged to Group 2 ( 6 to 6.5 ) and Group 3 (6.6 to 7) which is depicted in Table 3.
Table 3.
Maternal Hba1C with neonatal ABR results
| ABR | Maternal HbA1C | Total | |||
|---|---|---|---|---|---|
| Group 1 HbA1C < 6 | Group 2 HbA1C 6-6.5 | Group 3 HbA1C 6.6–7 | Group 4 HbA1C > 7 | ||
| B/L severe HL | 8 | 1 | 3 | 4 | 16 |
| B/L moderate HL | 2 | 4 | 6 | 3 | 15 |
| U/L Moderate HL(Right ear) | 0 | 1 | 1 | 0 | 2 |
We have studied the effect of maternal glycaemic level and hearing outcome of neonates by comparing ABR results of their neonates in each of the previously mentioned groups( 6, 6-6.5, 6.6 to 7, > 7). There number of neonates who underwent ABR test were 10,6,10 and 7 respectively in Group 1,2,3&group 4 respectively. ABR results of the neonates of each group is depicted in Table 3. The highest number of abnormal waveforms were observed in Group 1and Group 3. Both groups had 10 babies each, with abnormal ABR waveforms.
We didn’t observe any statistically significant association between maternal HbA1C levels and ABR abnormalities of their neonates. The case group had higher rate of caesarean deliveries(70 babies, 81.4%) compared to the control babies (44 babies, 51.1%),with a significant P value of 0.001.We didn’t find any significant association between coexistence of additional maternal risk factors like Hypertension (p value- 0.73), thyroid disease (p value − 0.75)and hearing status of the newborns.
Discussion
Diabetes mellitus is one of the most common metabolic disorder occurring during pregnancy with a prevalence of 16.9% [3]. The incidence of congenital hearing loss and ear abnormalities are higher in neonates of diabetic mothers [4]. There are multiple maternal factors like maternal infection during pregnancy such toxoplasmosis, rubella, CMV, and herpes, Maternal alcoholism, consanguineous marriage, perinatal hypoxia, ototoxic medications which can lead to congenital hearing loss [5].
The center for disease control and prevention has estimated the incidence of Gestational Diabetes Mellitus as 90% of all diabetic pregnancy, and remaining 10% being Overt Diabetes Mellitus(pre-existing diabetes) [6]. Diabetes Mellitus is the most commonly seen medical complication of pregnancy in south east Asia. The high circulating sugar levels and Insulin like Growth Factor (IGF − 1) in diabetic mothers have teratogenic effect resulting in auriculo oculo vertebral anomalies resulting in congenital hearing loss [7]. The first three months is the ideal period to screen the newborn, as early interventions and treatments ensures better prognosis [8]. This helps in the development of hearing system and improves the cognitive functions of the baby [9].
There are many proposed theories for the association between congenital hearing loss and maternal diabetes. Maternal hyperglycemia leads to higher levels of sugar and insulin like growth factor-1(IGF-1) in fetal circulation, which alters cochlear morphogenesis. There is increased generation of reactive oxygen species affecting organogenesis [10]. It is also stated that diabetes mellitus causes vascular damage of the developing inner ear by involvement of vestibulocochlear nerve, stria vascularis and hair cells. It was studied that the various parts of temporal bone including labyrinth, cochlear duct, the organ of Corti, striavascularis shows vascular congestion and hemorrhage [11].
In our study we observed a higher REFER status for the newborns of diabetic mothers in both ears, at first OAE (right ear 24%, left ear- 60.5%) and also in repeat OAE (right ear-38.2%, left ear-70.9%)compared to the normal controls, and the difference was statistically significant (p value on first OAE -right-0.008, left-0.002 and a p Value of 2nd OAE was 0.009 and 0.019 on right and left ear respectively).
The ABR report also showed higher percentage of greater hearing loss among cases compared to normal controls. The ABR results of cases showed higher percentage of greater hearing loss among them with 48.48% showing bilateral severe hearing loss and 45.45% showing bilateral moderate hearing loss and 6.06% showing unilateral moderate hearing loss (right ear). Whereas all the controls ( n = 5, 100%) who underwent ABR test had only bilateral mild hearing loss in our study. None of the controls showed moderate or severe hearing loss in our study compared to the case group, who showed only severe hearing loss and moderate hearing loss .
This study showed a significantly higher percentage of abnormal hearing outcome among neonates of diabetic mothers than non-diabetic mothers. The high percentage of abnormal hearing outcome among the case group confirms that maternal hyperglycemia has a strong negative influence on neonatal hearing. This could be because of the toxic effects of maternal hyperglycemia on developing auditory system of the fetus.
A study done by Maria Rina et al. to find the association between maternal Diabetes Mellitus and neonatal hearing among 150 neonates, showed a significant difference of 40% REFER status of OAE for newborns of diabetics, compared to 6% of newborns of non-diabetes [11]. Another study done by Lee Ja et al. on 311 children of diabetic pregnancy showed marked hearing loss in 71.1% of case group compared to controls ( 45.5% ) [12].
It is stated that poor maternal glycemic control can disrupt the organogenesis in first and second trimesters, but less commonly affects third trimester. When the fetus is subjected to inadequate metabolic control during the early organogenesis phase, the risk of congenital malformations and hearing loss is increased. Neonates of overt DM are exposed to higher levels of sugars for more duration hence hearing loss is more when compared to neonates of GDM [13]. However In our study, we didn’t observe any statistically significant difference among the hearing screening outcome between GDM and Overt diabetic group (p Value- 0.78) Considering the very low number of Overt DM(7%), we received in our study this result cannot be generalized.
In our study, on first day of birth, the case group had statistically significant lower mean sugar levels (61.10 mg/dl) compared to controls (73. 80 +/- 10.23 mg/dl ). Neonates of diabetic pregnancy are prone to frequent occurrence of neonatal hypoglycemia. Plasma glucose concentrations less than 40 mg/ dl is considered as neonatal hypoglycemia. However in this study none of the neonate had hypoglycemia, the lowest sugar value among case group was 42 mg/ dl and among control group, it was 48 mg/dl)
The excess glucose levels in fetus of diabatic mothers stimulate the fetal pancreatic B cells and release insulin, resulting in macrosomia [14]. In this study the case group showed higher birth weight (2.82+/-0.42 kg) than normal controls (2.75 kg). This points to frequent association of macrosomia complicating the diabetic pregnancies. A study done by Malang et al., observed a higher number of fetal complications like macrosomia, fetal distress and hypoglycemia, among newborns of diabetic mothers making them high risk pregnancy, requiring higher cesarean delivery and more ICU care [15].
We also observed higher mean APGAR score for case group ( 7.44 at 1 min, 9.51 at 5 min), than controls(6.97 at 1 min, 9.02at 5 min which was statistically significant (pvalue-0.001). This shows the incidence of respiratory distress among newborns of diabetic mothers .
In this study, the case group had significantly higher rate of caesarean deliveries (70 babies, 81.4%) compared to the control babies (44 babies, 51.1%). Similar results were observed in other studies [16]. Neonates of GDM show macrosomia, hypoglycemia, hypocalcemia, polycythemia, hyperbilirubinemia, respiratory distress syndrome, and congenital malformations which leads to higher incidence of delivery by caesarean section in them [17].
The physiologic alterations of diabetes during pregnancy include alterations in the mother’s lipids, amino acids, and glucose levels, which prevent the developing fetus from getting these vital substrates. Diabetes causes mothers to become obese and suffer cardiovascular illnesses. Newborns of diabetic mothers require more ICU care, due to increased risk of associated complications including transient tachypnoea [18].
A recent study by Benner et al. observed increased prevalence of Diabetes Mellitus in young mothers. The associated neonatal complications were higher incidence of congenital deafness, sensorineural hearing loss, ear deformities, and also GDM mothers had higher incidence of pre-eclampsia and caesarian section [19]. The physiological adaptability of both mother and fetus are changed by diabetes .
In the present study, we observed the neonates of diabetic mothers had a significant higher rate of abnormal hearing outcome when compared to neonates of non-diabetic mothers. Also birth by caesarean section, increased birth weight, lower sugar levels, and higher APGAR scores. All are suggestive of the neonatal complications of diabetic pregnancies. There are limited studies on hearing loss of neonates and maternal hyperglycemic status. Majority of the available literature states that maternal hyperglycemia is a potential risk factor for development of neonatal hearing loss. Our study observed that the neonates of diabetic mothers are at the increased risk of congenital hearing loss compared to normal controls by ABR test as 96% of the cases had bilateral moderate or severe hearing loss whereas all the tested controls were showing only mild bilateral hearing loss. The neonates of diabetic mothers are also prone for frequent association of complications like preterm birth, macrosomia, respiratory distress and neonatal hypoglycemia.
Conclusion
This study concludes that maternal diabetes mellitus is a potential risk factor for hearing abnormalities in newborns. Uncontrolled maternal glucose levels can affect the developing auditory system. Routine neonatal hearing screening tools like OAE and ABR test will help in early identification of the babies having hearing loss. This study emphasis the need for better glycaemic control in diabetic pregnancy, the importance of early and mandatory hearing screening in newborns of diabetic mothers and also to initiate the hearing rehabilitation and interventions at the earliest for those with hearing impairment.
Acknowledgements
Ms. Megha, statistician for helping the statistical analysis.
Author Contribution
Amrutha P: Design, Literature search, data acquisition, data analysis, manuscript preparation, manuscript editing. Nayana V G: concept, study design, definition of intellectual content, Data analysis ,manuscript editing, manuscript review. Nimalka Maria Sequeira: study design, data analysis, manuscript review. Hemaraj Nayaka S: Data analysis, statistical analysis, manuscript review.
Funding
This study is self funded.
Declarations
Conflict of Interest
Dr. Amrutha P, Dr. Nayana V G, Ms. Nimalka Maria Sequeria and Mr. Hemaraj Nayaka S declare they have no conflict of interest.
Ethics Approval
Ethics approval obtained from institutional ethics committee (Yenepoya ethics committee) YEC2/706
Informed Consent
Informed Consent taken from all participants.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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