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Effects of ambient air pollution, fresh fruit and vegetable intakes as well as maternal psychosocial stress on the outcome of newborn otoacoustic emission hearing screening

Abstract

Background

Newborn hearing screening results indicated that more than 40% of the detected infants had no recognized risk factors. To determine whether maternal exposure to ambient air pollutants and experience of stressful life event, as well as lack of fresh fruit and vegetable during pregnancy are associated with the abnormal hearing development among newborns.

Methods

A total of 1193 newborns and their mothers were recruited in this study. Personal information and covariates were collected by face to face interview. Medical examination results of newborns and their mothers were extracted from medical record. We estimated personal air pollutant exposure level through inverse distance weighted method based on data from air quality monitoring stations and assessed the auditory development of newborns via distortion product otoacoustic emission (DPOAE). Unconditional logistic regression model was used to estimate the relationship between DPOAE screening result and the potential influential factors as well as the combined effect.

Results

The results indicated that PM10 exposure during the second trimester and stressful life event during the third trimester could increase the risk of not passing DPOAE test among newborns. However, frequent intakes of fruit and vegetable significantly reduced the risk. There was a synergetic interaction between PM10 exposure and stressful life event on neonatal hearing development.

Conclusions

To alleviate abnormal auditory development among fetus, pregnant woman should decrease the exposures to ambient air pollutant and negative life event and at the same time, intake sufficient fresh fruit and vegetable.

Peer Review reports

Background

Hearing impairment is one of the most common congenital anomaly at birth, constituting a serious obstacle to the developments of language and intelligence. It has also been documented to be associated with poor academic performance in school life as well as limited access to employment and social interaction in adulthood [1]. The incidence of newborn hearing loss was reported between 2 and 15% in births with abnormal conditions while 0.3% in healthy births [2, 3]. In order to alleviate the obstacle to personal development as well as the burdens on family and society, many counties in the world launch universal neonatal hearing screening project to ensure a prompt identification and rehabilitation of these infants. Meanwhile, pediatricians are dedicated to exploring and identifying the risk factors for hearing impairment in newborns, thus contributing to the effective intervention at an even earlier stage. Family history, congenital infections, craniofacial anomalies and other factors were identified successively and added to the typical risk factor list for routine screening [4]. However, a growing number of investigations found that more than 40% of the detected infants lacked these recognized risk factors or the association between these risk factors and congenital hearing impairment lacked statistical significance [4, 5].

Hearing development, containing neurosensory as well as conductive components, begins in early fetal life and becomes mature several months after birth [6]. The developmental period of hearing in utero is closely correlated to the maturity of central nervous system, which is affected by maternal environmental exposure in gestation. A recently published systematic review suggested an inverse association between maternal air pollutant exposure and head circumference at birth [7]. Also, our previous investigation indicated that the PM2.5 exposure in trimester 2 was negatively associated with neurological behavior score in newborns[8]. Oxidative damage and neuroinflammation were revealed by toxicological research as the main plausible mechanisms [9, 10]. In this context, prenatal exposure to air pollution may also affect auditory development of fetus, but the evidence remains limited. Besides, maternal psychological distress over pregnancy was suggested as a key adverse factor for fetal neurological development, for example, exhibiting a negative effect on fetal vision maturity [11]. It was also reported to be associated with alterations in fetal cortical gyrification, hippocampal volume and metabolite level of neurotransmitter, respectively [12]. A recent research found that antenatal maternal anxiety trait exerted an adverse effect on fetal middle cerebral artery plasticity and consequently led to poor nutrient and oxygen supply to the developing embryonic brain [13]. Therefore, maternal psychosocial condition probably play a role in the embryonic auditory development as well. Fruit and vegetable intakes during gestation were reported to be positively associated with the biparietal diameter of newborns [14]. As excellent sources of folate and vitamin C [14, 15], consumptions of fruit and vegetable are probably essential for cell division via transferring and processing one-carbon in DNA synthesis process [16], and exert a significant protective effect on vision and olfaction against ionizing radiation during neurulation in rodent model[17]. Given that vitamin C is a pivotal contributor to the redox homeostasis, deficiency of fruit and vegetable in maternal diet was probably linked to the increase of oxidative damage in the developing nervous system [18].

As there are similar biological mechanisms through which ambient air pollutant exposure, maternal stress and fruit and vegetable intakes influence the developing nervous system, combined exposure may lead to synergistic or antagonize effects. Therefore, in the present study, we enrolled a total of 1190 healthy pregnant women, and collected information via structural questionnaire and medical record, on the one hand, to elucidate the individual association of air pollutant, maternal distress and fruit and vegetable intakes with newborn hearing screening outcomes, on the other hand, to assess the potential combined effects of air pollutant, maternal distress and fruit and vegetable intakes on hearing development.

Methods

Study design and population

This population-based prospective investigation was conducted in Changsha city, Hunan province, which was previously reported elsewhere [8]. A total of 1190 healthy pregnant women were enrolled in this study in 2017, who had been lived in Changsha for at least 1 year and registered in Hunan Maternal and Child Health Hospital for delivery. As we focused on the effect of living environment on hearing screening result, pregnant woman with occupational exposure such as dust and excessive noise were excluded. During the routine antenatal examination, maternal life stressor, anxiety and depression were assessed by Life Events Scale of Pregnant Woman (LESPW) [19], Spielberger State-Trait Anxiety Inventory (STAI) [20] and Edinburgh Postnatal Depression Scale (EPDS), respectively [21]. LESPW contains 53 items and divides into subjective event (SE) and objective event (OE). OE is further divides into three grades, OE1, OE2 and OE3. The thresholds of SE, OE1, OE2 and OE3 were 130, 310, 225 and 1450, respectively. STAI is designed to assess state anxiety and traint anxiety through 40 items and the threshold scores were set at 39 and 41 in this investigation, respectively. EPDS contains 10 items and score equal to or higher than 9 is considered as depression. If intake frequency of fruit or vegetable was less than once a month, we defined it as no fruit or vegetable intake. After childbirth, we conducted a face to face questionnaire survey among the participants. The questionnaire contained basic information and potential confounding factors, including maternal age, height, weight before pregnancy, reproductive history, medical history during pregnancy, period of residence in Changsha, food intake frequent, parent's smoking habit (including passive smoking), alcohol intake and home address. Particularly, we pay attention to the factors related to indoor air pollution (kitchen fuel, house decoration during pregnancy and passive smoking) and dietary habit (intake of fruit, vegetable, milk, soy milk and tea). After finish the interview, all the participants signed the written informed consent. The research protocol and process have been approved by the ethics committee of Xiangya School of Public Health, Central South University.

Estimation of exposure to ambient air pollutants

In this study, we used data from Changsha City Air Quality Monitoring Station to assess the maternal exposure level of air pollutants during pregnancy. There are ten monitoring stations in the urban area of ​​Changsha, recording the concentrations of five kinds of atmospheric pollutants (PM10, PM2.5, CO, NO2, SO2). Daily average concentrations of the five pollutants and Inverse Distance Weighted (IDW) were used in the estimation of individual exposure level [22]. IDW selects the concentrations from the four nearest monitoring points to the maternal home address. At the same time, satellite map is used to measure the straight-line distance (d1 to d4) from the four monitoring points to the maternal address. The specific calculation formula is as follows:

$$C=\frac{\frac{1}{{\mathrm{d}}_{1}^{2}}\times {\mathrm{c}}_{1}+\frac{1}{{\mathrm{d}}_{2}^{2}}\times {\mathrm{c}}_{2}+\frac{1}{{\mathrm{d}}_{3}^{2}}\times {\mathrm{c}}_{3}+\frac{1}{{\mathrm{d}}_{4}^{2}}\times {\mathrm{c}}_{4}}{\frac{1}{{\mathrm{d}}_{1}^{2}}+\frac{1}{{\mathrm{d}}_{2}^{2}}+\frac{1}{{\mathrm{d}}_{3}^{2}}+\frac{1}{{\mathrm{d}}_{4}^{2}}}$$

Hearing screening for newborns

Distortion product otoacoustic emission (DPOAE) was employed to assess the auditory development of newborns via otoacoustic emission screening instrument (GSI70, USA). Parameters were set as following: f2 / f1 = 1.22, stimulus intensity L1 = 65 dB SPL, L2 = 55 dB SPL, frequency range (represented by f2) f2 = 1.5, 2.0, 3.0, 4.0, 5.0, 6.0 kHz, average time = 4 s. Inspection process was carried out in a soundproof shielded room when newborn was in a quiet state. Before screening, investigator should confirm that the newborn's external auditory meatus is free of foreign matter, and then select the suitable probe adapting to the newborn's external auditory. The instrument displays the result as PASS or NOT PASS. Both ears of the newborn are subject to DPOAE test, and as long as one ear fails the test, it is recognized as not passed. This screening is carried out by a well-trained investigator who does not know about the information of newborn. A warm and quiet area was chosen for screening test and before test, investigator examine the external auditory canalfor debris, wax etc.

Statistical analysis

Continuous variables were expressed as mean ± standard deviation, and categorical variables were expressed in terms of frequency and percentage. A total of 1190 newborns were divided into group "PASS" and group "NOT PASS" according to the DPOAE screening result. Chi-square test and Mann–Whitney U test were used to compare the distribution differences of diverse variables between two groups.

Logistic regression model was used for estimation the relationship between DPOAE screening result and the potential influential effecters. In the univariate analysis, only the exposure levels of PM10 and PM2.5 were found to be statistically associated with screening outcome among five air pollutants, Therefore, we only included the levels of PM10 and PM2.5 in the form of quartile into multivariable model, which was adjusted by maternal age, paternal age, maternal educational level, premature delivery, newborn sex, birthweight, instrument assist in child delivery and amnionic fluid status. And the results were displayed as odds ratio (OR) and 95% confidence interval (95% CI).

In the interaction analysis, the concentrations of PM10 and PM2.5 were converted into low and high groups by the corresponding medians, and low exposure group was used as reference. Logistic regression model was applied to estimate the association of screening result with fruit or vegetable intake, mental stimulation and parity respectively after stratification. We established an interaction term in the analysis of overall data and gave the p value as interaction p value.

All analyses were performed using SPSS 22.0. The estimated value, its 95% CI and p value were given in the results, and P < 0.05 was considered statistically significant.

Results

Among the 1190 newborns, 166 (13.9%) did not pass the DPOAE test. The distribution and statistical analysis results of the variables in the not pass and pass group were shown in Table 1. We observed that the differences of parity, stressful life event during pregnancy, and prenatal exposure to PM10 and PM2.5 were statistically different between the two groups (P < 0.05), which may be potential risk factors for newborn not passing DPOAE test. As intake frequencies of fruit and vegetable less than once a month and experience of stressful life event were rare in real life situation, the number of pregnant woman with these characteristics was relatively small.

Table 1 Demographic information, covariates and personal air pollutant exposure level between pass and not pass of DPOAE test groups (n = 1190)

Table 2 summarizes the average exposure concentrations of PM10, PM2.5, CO, NO2 and SO2 among pregnant women in the first, second and third trimesters. The first trimester had the highest exposures level of the five air pollutants and the corresponding average levels were 80.58 μg/m, 49.15 μg/m3, 1.05 mg/m3, 40.17 μg/m3 and 14.56 μg/m3. While the second trimester had the lowest exposure levels of air pollutants and the average levels were PM10 57.31 μg/m, PM2.5 33.34 μg/m3, CO 0.94 mg/m3, NO2 30.82 μg/m3 and SO2 13.59 μg/m3.

Table 2 Descriptive statistics for air pollution during different time windows attributed to pregnancy women (n = 1190)

Association between exposures to atmospheric pollutants during pregnancy and DPOAE test results of newborns was estimated by univariable and multivariable logistic regression analysis and the results were displayed in Table 3. The concentration of PM10 in the second trimester significantly increased the risk of losing the test with crude OR of 1.305 (95% CI, 1.117, 1.524), which was robust to the adjustment of parental age, maternal education level, premature, sex, birthweight, dietary habit, anxiety, depression, life event, indoor air pollution and et al. As for PM2.5, the level in the second trimester was significantly associated with increased risk of not passing DPOAE test with crude OR of 1.207 (95% CI, 1.028, 1.417). However, the significance alleviated into null after adjustment of potential covariables.

Table 3 Odds ratio (95% CI) of not passing DPOAE test for exposure to PM10 and PM2.5 during different time windows (n = 1190)

As Table 4 showed, indoor air pollution including smoking, house renovation and kitchen fuel seemed to have no evident effect on the risk of losing the screening test.

Table 4 Odds ratio (95% CI) of not passing DPOAE test for exposure to indoor air pollution during the whole pregnancy period (n = 1190)

Newborns with mother experiencing stressful life event during the 3rd trimester had more than 3 times higher risk of not passing DPOAE test with crude OR of 3.568 (95% CI, 1.266, 10.055) and adjusted OR of 3.217 (95% CI, 1.080, 9.581), 3.366 (95% CI, 1.097, 10.330), 3.678 (95% CI, 1.183, 11.433) in different adjusted models (Table 5). Conversely, pregnant mother with regular intake of fruit and vegetable would decrease the risk of not passing the test and the association remained significant after adjustment of parental age, maternal education level, premature, parity, sex, birth weight, amniotic fluid condition, PM 2.5 and PM10.

Table 5 Odds ratio (95% CI) of not passing DPOAE test for dietary habits and stressful life event during pregnancy period (n = 1190)

After stratification by the medians of PM2.5 or PM10, we found that frequent intake of fruit and vegetable significantly reduced the risk of losing DPOAE test only among mother with low exposure level of PM2.5 and PM10. Stressful life event during pregnancy significantly increased the risk of not passing DPOAE test by 4 time sonly for newborns with higher prenatal exposure level of PM10 (OR, 4.242, 95% CI, 1.742, 10.329, interaction p value = 0.033) (Table 6).

Table 6 Combined effects of air pollutant and other risk factors on the results of DOPAE test among newborns (n = 1190)

Discussion

Our results show that PM10 exposure during the second trimester and stressful life event during the third trimester could increase the risk of not passing DPOAE test among newborns, while frequent intakes of fruit and vegetable significantly reduced the risk. Notably, a synergetic interaction was found between PM10 exposure and stressful life event on neonatal hearing development. To the best of our knowledge, this is the first epidemiological study to elucidate the effects of PM10, stressful life event and intakes of fruit and vegetable during pregnancy on auditory development among human fetus.

PM10 is known as a kind of inhalable particle with aerodynamic diameter of 10 microns or less, and it can enter the human respiratory tract, inducing systematic inflammation [23] and oxidative damage to both mother and fetus[24]. Evidence related to the adverse effect of prenatal exposure of PM10 on auditory development is limited. However, a couple of epidemiological investigation consistently reported the positive association between prenatal exposure to tobacco smoke and risk of hearing impairment among children or adolescent [25, 26]. It is worthy noting that PM10 has a large surface area and can absorb a variety of harmful substances, such as polychlorinated biphenyls (PCBs), dioxins and heavy metals [27, 28]. PCBs are considered as neurotoxic substances and could incur abnormal hearing development [29,30,31,32,33]. A study from central Taiwan reported that newborns had an increased risk of raising low-frequency hearing threshold due to exposure to PCBs from contaminated rice oil [29].Dioxin is a ubiquitous persistent environmental pollutant and in animal model, it increased cochlear sensitivity threshold at 1.5 months of age due to low dose exposure in embryonic stage [34]. Therefore, particulate matter itself and the adsorbed component could both contribute to the impairment of hearing development among newborns.

Negative life event during pregnancy could elicit stress status among pregnant woman, which is a systemic non-specific adaptive response and associated with increased incidence of brain development disorder in offspring [35] as well as pregnancy complication among pregnant woman [36, 37]. Investigators found that psychological trauma experienced in pregnancy, for example, destruction of the World Trade Center in 2001, was negatively associated with newborn head circumference, implying the potential influence on fetal neurological development [38, 39]. In rodent model, prenatal stress was reported eliciting diversity of neuropsychological impairments among offspring, which was due to the disturbance in early brain development programming [40]. Notably, Kadner and colleagues found that exposure of pregnant rats to prenatal stress could increase the low-frequency hearing threshold of male offspring, probably through accelerating cochlear degeneration and/or disrupting cochlear development [41]. In line with the above-mentioned research, we observed a positive association of prenatal stressful life event with risk of failure in auditory screening test. However, few study elucidated the underlying mechanism. A growing number of literatures suggested the possible involvement of oxidative stress in the association between maternal psychological stress and fetal hearing impairment [42, 43]. Oxidative damage was one of the most widely accepted pathogenic mechanism underlying diverse birth deficits or disorder, and played a key role in hearing impairment caused by heavy metal and noises [44, 45]. In this context, oxidative stress could be one of the plausible mechanisms for the adverse effect of prenatal psychological stress on fetal auditory development.

Hearing loss usually occur accompanied with folic acid-deficient condition [46]. At the same time, folic acid supplementation can improve the outcome of hearing loss, which is related to the preventions of inner ear collagen deposition and oxidative stress [47]. In addition, vitamin C, a kind of non-enzymatic antioxidants, exerted a protective effect against impairment in hearing threshold induced by ototoxic drugs in experimental mice [48] and in epidemiological study, it was negatively correlated to hearing impairment among both diabetes patient and control group [49]. In the present study, consumption of fruit and vegetable during pregnancy could increase the pass rate of DPOAE, which may be related to the protective effects of folic acid and vitamin C in fruit and vegetable. In analysis of interaction, we found that in PM10 and PM2.5 low exposure groups, intake of fruit and vegetable during pregnancy showed a significant protective effect for hearing development while this effect alleviated to null in high exposure group. It may be due to the higher level of oxidative stress in the PM2.5 and PM10 high-exposed group, which could not be reversed by the antioxidant component in fruit and vegetable. Also, experience of stressful life event during pregnancy significantly increased higher risk of losing DPOAE among newborns with high level of prenatal PM10 exposure as compared to the low exposed group, which was probably attributed to the synergetic oxidative damages from both stressful life event and high level of PM10 exposure.

A growing number of literatures reported the adverse effect of smoking and passive smoking on hearing impairment among fetus, children and adults [50,51,52], which was in line with the result from animal research [53]. However, in our study, we failed to find a correlation between cigarette exposure and DPOAE result, which may be due to the extremely low proportion of mother who were exposed to second-hand smoke or smoked during pregnancy.

In the present study, we applied otoacoustic emission (OAE) screening test to detect infants with hearing impairment. OAE originates from normal cochlear activity and can also be inspired by sound stimulation, which releases outwards through ossicular chain, tympanic membrane and external auditory meatus. The signal can be detected by instrument and any abnormalities in ossicular chain, tympanic membrane and external auditory meatus will result in fail in screening test. OAE examination is the most commonly used method of newborn hearing screening in pediatric clinics, and it has the advantages of rapid, accurate and non-invasive [54, 55]. A total of 13.4% participants in the present study did not pass the test, which was much higher than the results from Singapore [56] and UK [57], but lower than the screening outcome from India [58]. As a neonatal hearing screening tool, optoacoustic emissions along with auditory brainstem responses (ABRs) could not perform without error. Although, more reliable frequency range was applied in the present study, the false positive rate was estimated to be 8%according to published literature [59, 60]. Therefore, diagnostic hearing impairment is warranted in the following study to confirm these findings.

Besides, this study has other limitations. Personal exposure to ambient air pollutant was estimated via air monitoring data from government websites by IDW method, without considering the influence of activity pattern, which would misclassified the exposure grades. Besides, the concentrations of PCBs, dioxins and heavy metals in PM10 were not be measured in this study.

Conclusions

The present investigation indicated that PM10 and stressful life event during pregnancy would increase the risk of not passing newborn otoacoustic emission hearing screening. However, sufficient consumptions of fruit and vegetable could reduce the risk. In addition, there was a synergetical effect between PM10 and stressful life event on neonatal hearing development. Therefore, to alleviate abnormal auditory development of fetus, pregnant woman should avoid exposure to ambient air pollutant and experience of negative life event and at the same time, intake sufficient fresh fruit and vegetable.

Availability of data and materials

The datasets used and analysed in the current study were available from the corresponding author on reasonable request.

Abbreviations

LESPW:

Life Events Scale of Pregnant Woman

STAI:

Spielberger State-Trait Anxiety Inventory

EPDS:

Edinburgh Postnatal Depression Scale

DPOAE:

Distortion product otoacoustic emission

References

  1. Launch of the World Report on Hearing [https://www.who.int/news-room/events/detail/2021/03/03/default-calendar/launch-of-the-world-report-on-hearing]

  2. Cross CP, Liao S, Urdang ZD, Srikanth P, Garinis AC, Steyger PS. Effect of sepsis and systemic inflammatory response syndrome on neonatal hearing screening outcomes following gentamicin exposure. Int J Pediatr Otorhinolaryngol. 2015;79(11):1915–9.

    PubMed  PubMed Central  Article  Google Scholar 

  3. Shahid R, Vigilante M, Deyro H, Reyes I, Gonzalez B, Kliethermes S. Risk Factors for Failed Newborn Otoacoustic Emissions Hearing Screen. Clin Pediatr. 2016;55(12):1138–42.

    Article  Google Scholar 

  4. Vohr BR, Widen JE, Cone-Wesson B, Sininger YS, Gorga MP, Folsom RC, Norton SJ. Identification of Neonatal Hearing Impairment: Characteristics of Infants in the Neonatal Intensive Care Unit and Well-Baby Nursery. Ear Hear. 2000;21(5):373–82.

    CAS  PubMed  Article  Google Scholar 

  5. Langagne T, Leveque M, Schmidt P, Chays A. Universal newborn hearing screening in the Champagne-Ardenne region: a 4-year follow-up after early diagnosis of hearing impairment. Int J Pediatr Otorhinolaryngol. 2010;74(10):1164–70.

    CAS  PubMed  Article  Google Scholar 

  6. Clark-Gambelunghe MB, Clark DA. Sensory development. Pediatr Clin North Am. 2015;62(2):367–84.

    PubMed  Article  Google Scholar 

  7. Carvalho MA, Hettfleisch K, Rodrigues AS, Benachi A, Vieira SE, Saldiva S, Saldiva PHN, Francisco RPV, Bernardes LS. Association between exposure to air pollution during intrauterine life and cephalic circumference of the newborn. Environ Sci Pollut Res Int. 2021;28(8):9701–11.

    CAS  PubMed  Article  Google Scholar 

  8. Chen B, Huang S, He J, He Q, Chen S, Liu X, Peng S, Luo D, Duan Y. Sex-specific influence of prenatal air pollutant exposure on neonatal neurobehavioral development and the sensitive window. Chemosphere. 2020;254:126824.

    CAS  PubMed  Article  Google Scholar 

  9. Schulz H, Karrasch S, Bolke G, Cyrys J, Hornberg C, Pickford R, Schneider A, Witt C, Hoffmann B. Breathing: Ambient Air Pollution and Health - Part III. Pneumologie. 2019;73(7):407–29.

    CAS  PubMed  Article  Google Scholar 

  10. Bolton JL, Smith SH, Huff NC, Gilmour MI, Foster WM, Auten RL, Bilbo SD. Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner. FASEB J. 2012;26(11):4743–54.

    CAS  PubMed  Article  Google Scholar 

  11. Reissland N, Wood R, Einbeck J, Lane A. Effects of maternal mental health on fetal visual preference for face-like compared to non-face like light stimulation. Early Hum Dev. 2020;12:151.

    Google Scholar 

  12. Wu Y, Lu YC, Jacobs M, Pradhan S, Kapse K, Zhao L, Niforatos-Andescavage N, Vezina G, du Plessis AJ, Limperopoulos C. Association of Prenatal Maternal Psychological Distress With Fetal Brain Growth, Metabolism, and Cortical Maturation. JAMA Netw Open. 2020;3(1):e1919940.

    PubMed  PubMed Central  Article  Google Scholar 

  13. Bayrak M, Sancak A. Association between antenatal maternal anxiety and fetal middle cerebral artery Doppler depends on fetal gender. J Matern Fetal Neonatal Med. 2021;34(5):818–23.

    CAS  PubMed  Article  Google Scholar 

  14. Jang W, Kim H, Lee BE, Chang N. Maternal fruit and vegetable or vitamin C consumption during pregnancy is associated with fetal growth and infant growth up to 6 months: results from the Korean Mothers and Children’s Environmental Health (MOCEH) cohort study. Nutr J. 2018;17(1):105.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. Koebnick C, Heins UA, Hoffmann I, Dagnelie PC, Leitzmann C. Folate Status during Pregnancy in Women Is Improved by Long-term High Vegetable Intake Compared with the Average Western Diet. J Nutr. 2001;131(3):733–9.

    CAS  PubMed  Article  Google Scholar 

  16. van Gool JD, Hirche H, Lax H, De Schaepdrijver L. Folic acid and primary prevention of neural tube defects: A review. Reprod Toxicol. 2018;80:73–84.

    PubMed  Article  CAS  Google Scholar 

  17. Craenen K, Verslegers M, Callaerts-Vegh Z, Craeghs L, Buset J, Govaerts K, Neefs M, Gsell W, Baatout S, D’Hooge R, et al. Folic Acid Fortification Prevents Morphological and Behavioral Consequences of X-Ray Exposure During Neurulation. Front Behav Neurosci. 2020;14:609660.

    CAS  PubMed  Article  Google Scholar 

  18. Paidi MD, Schjoldager JG, Lykkesfeldt J, Tveden-Nyborg P. Prenatal vitamin C deficiency results in differential levels of oxidative stress during late gestation in foetal guinea pig brains. Redox Biol. 2014;2:361–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Yan G, Yu-feng Y, Qi H, Tai-zhen H, Kai-nan Y. Development of life events scale for pregnant women and analysis of its reliability and validity. Chinese J Woman Child Health Res. 2010;6(21):743–6.

    Google Scholar 

  20. Gaudry E, Vagg P, Spielberger CD. Validation of the State-Trait Distinction in Anxiety Research. Multivar Behav Res. 1975;10(3):331–41.

    CAS  Article  Google Scholar 

  21. Cox JL, Holden JM, Sagovsky R. Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. Br J Psychiatry. 1987;150:782–6.

    CAS  PubMed  Article  Google Scholar 

  22. Deng Q, Lu C, Norback D, Bornehag CG, Zhang Y, Liu W, Yuan H, Sundell J. Early life exposure to ambient air pollution and childhood asthma in China. Environ Res. 2015;143(Pt A):83–92.

    CAS  PubMed  Article  Google Scholar 

  23. Buxton MA, Perng W, Tellez-Rojo MM, Rodriguez-Carmona Y, Cantoral A, Sanchez BN, Rivera-Gonzalez LO, Gronlund CJ, Shivappa N, Hebert JR, et al. Particulate matter exposure, dietary inflammatory index and preterm birth in Mexico city. Mexico Environ Res. 2020;189:109852.

    CAS  PubMed  Article  Google Scholar 

  24. Grevendonk L, Janssen BG, Vanpoucke C, Lefebvre W, Hoxha M, Bollati V, Nawrot TS. Mitochondrial oxidative DNA damage and exposure to particulate air pollution in mother-newborn pairs. Environ Health. 2016;15:10.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  25. Wilunda C, Yoshida S, Tanaka S, Kanazawa Y, Kimura T, Kawakami K. Exposure to tobacco smoke prenatally and during infancy and risk of hearing impairment among children in Japan: A retrospective cohort study. Paediatr Perinat Epidemiol. 2018;32(5):430–8.

    PubMed  Article  Google Scholar 

  26. Weitzman M, Govil N, Liu YH, Lalwani AK. Maternal prenatal smoking and hearing loss among adolescents. JAMA Otolaryngol Head Neck Surg. 2013;139(7):669–77.

    PubMed  Google Scholar 

  27. Fu S, Cheng HX, Liu YH, Yang ZZ, Xu XB. Spatial character of polychlorinated biphenyls from soil and respirable particulate matter in Taiyuan. China Chemosphere. 2009;74(11):1477–84.

    CAS  PubMed  Article  Google Scholar 

  28. Dickerson AS, Rahbar MH, Bakian AV, Bilder DA, Harrington RA, Pettygrove S, Kirby RS, Durkin MS, Han I, Moye LA 3rd, et al. Autism spectrum disorder prevalence and associations with air concentrations of lead, mercury, and arsenic. Environ Monit Assess. 2016;188(7):407.

    PubMed  Article  CAS  Google Scholar 

  29. Li MC, Wu HP, Yang CY, Chen PC, Lambert GH, Leon Guo Y. Gestational exposure to polychlorinated biphenyls and dibenzofurans induced asymmetric hearing loss: Yucheng children study. Environ Res. 2015;137:65–71.

    CAS  PubMed  Article  Google Scholar 

  30. Grandjean P, Landrigan PJ. Developmental neurotoxicity of industrial chemicals. The Lancet. 2006;368(9553):2167–78.

    CAS  Article  Google Scholar 

  31. Trnovec T, Sovcikova E, Pavlovcinova G, Jakubikova J, Jusko TA, Hustak M, Jureckova D, Palkovicova L, Kocan A, Drobna B, et al. Serum PCB concentrations and cochlear function in 12-year-old children. Environ Sci Technol. 2010;44(8):2884–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. Powers BE, Poon E, Sable HJ, Schantz SL. Developmental exposure to PCBs, MeHg, or both: long-term effects on auditory function. Environ Health Perspect. 2009;117(7):1101–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. Dai Q, Min X, Weng M. A review of polychlorinated biphenyls (PCBs) pollution in indoor air environment. J Air Waste Manag Assoc. 2016;66(10):941–50.

    CAS  PubMed  Article  Google Scholar 

  34. Safe TM, Luebke AE. Prenatal low dosage dioxin (TCDD) exposure impairs cochlear function resulting in auditory neuropathy. Hear Res. 2016;331:7–12.

    CAS  PubMed  Article  Google Scholar 

  35. Dowell J, Elser BA, Schroeder RE, Stevens HE. Cellular stress mechanisms of prenatal maternal stress: Heat shock factors and oxidative stress. Neurosci Lett. 2019;709: 134368.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. Gray SAO, Jones CW, Theall KP, Glackin E, Drury SS. Thinking Across Generations: Unique Contributions of Maternal Early Life andPrenatal Stress to Infant Physiology. J Am Acad Child Adolesc Psychiatry. 2017;56(11):922–9.

    PubMed  PubMed Central  Article  Google Scholar 

  37. Panetta P, Berry A, Bellisario V, Capoccia S, Raggi C, Luoni A, Longo L, Riva MA, Cirulli F. Long-Term Sex-Dependent Vulnerability to Metabolic challenges in Prenatally Stressed Rats. Front Behav Neurosci. 2017;11:113.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  38. Davydov DM, Lobanov AV, Morozov SG, Gribova IE, Murashev AN. Neurodevelopment and phenotype-modulating functions of S100B protein: a pilot study. Physiol Behav. 2015;140:188–96.

    CAS  PubMed  Article  Google Scholar 

  39. Engel SM, Berkowitz GS, Wolff MS, Yehuda R. Psychological trauma associated with the World Trade Center attacks and its effect on pregnancy outcome. Paediatr Perinat Epidemiol. 2005;19(5):334–41.

    PubMed  Article  Google Scholar 

  40. Bengoetxea X, Paternain L, Martisova E, Milagro FI, Martinez JA, Campion J, Ramirez MJ. Effects of perinatal diet and prenatal stress on the behavioural profile of aged male and female rats. J Psychopharmacol. 2017;31(3):356–64.

    PubMed  Article  Google Scholar 

  41. Kadnera A, Pressimone VJ, Lally BE, Salm AK, Berrebi AS. Low-frequency hearing loss in prenatally stressed rats. NeuroReport. 2006;17(6):635–8.

    Article  Google Scholar 

  42. Zhu Z, Li X, Chen W, Zhao Y, Li H, Qing C, Jia N, Bai Z, Liu J. Prenatal stress causes gender-dependent neuronal loss and oxidative stress in rat hippocampus. J Neurosci Res. 2004;78(6):837–44.

    CAS  PubMed  Article  Google Scholar 

  43. Cao K, Zheng A, Xu J, Li H, Liu J, Peng Y, Long J, Zou X, Li Y, Chen C, et al. AMPK activation prevents prenatal stress-induced cognitive impairment: modulation of mitochondrial content and oxidative stress. Free Radical Biol Med. 2014;75:156–66.

    CAS  Article  Google Scholar 

  44. Rosati R, Jamesdaniel S. Chronic Lead Exposure Induces Cochlear Oxidative Stress and Impairs Hearing. Free Radical Biol Med. 2017;112:73.

    Article  Google Scholar 

  45. Liu Y, Ao L, Li Y, Zhao Y, Wen Y, Ding H. The SIRT2 inhibitor AK-7 decreases cochlear cell apoptosis and attenuates noise-induced hearing loss. Biochem Biophys Res Commun. 2019;509(3):641–6.

    CAS  PubMed  Article  Google Scholar 

  46. Martinez-Vega R, Garrido F, Partearroyo T, Cediel R, Zeisel SH, Martinez-Alvarez C, Varela-Moreiras G, Varela-Nieto I, Pajares MA. Folic acid deficiency induces premature hearing loss through mechanisms involving cochlear oxidative stress and impairment of homocysteine metabolism. FASEB J. 2015;29(2):418–32.

    CAS  PubMed  Article  Google Scholar 

  47. Kundu S, Munjal C, Tyagi N, Sen U, Tyagi AC, Tyagi SC. Folic acid improves inner ear vascularization in hyperhomocysteinemic mice. Hear Res. 2012;284(1–2):42–51.

    CAS  PubMed  Article  Google Scholar 

  48. Zadrozniak M, Szymanski M, Luszczki JJ. Vitamin C alleviates ototoxic effect caused by coadministration of amikacin and furosemide. Pharmacol Rep. 2019;71(2):351–6.

    CAS  PubMed  Article  Google Scholar 

  49. Aladag I, Eyibilen A, Guven M, Atis O, Erkorkmaz U. Role of oxidative stress in hearing impairment in patients with type two diabetes mellitus. J Laryngol Otol. 2009;123(9):957–63.

    CAS  PubMed  Article  Google Scholar 

  50. Hu H, Sasaki N, Ogasawara T, Nagahama S, Akter S, Kuwahara K, Kochi T, Eguchi M, Kashino I, Murakami T, et al. Smoking, Smoking Cessation, and the Risk of Hearing Loss: Japan Epidemiology Collaboration on Occupational Health Study. Nicotine Tob Res. 2019;21(4):481–8.

    PubMed  Article  Google Scholar 

  51. Chang J, Ryou N, Jun HJ, Hwang SY, Song JJ, Chae SW. Effect of Cigarette Smoking and Passive Smoking on Hearing Impairment: Data from a Population-Based Study. PLoS ONE. 2016;11(1):e0146608.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  52. Durante AS, Nascimento CMD, Lopes C. Otoacoustic emissions in neonates exposed to smoke during pregnancy. Braz J Otorhinolaryngol. 2021;87(2):193–9. https://doi.org/10.1016/j.bjorl.2019.08.001. Epub 2019 Sept.

  53. Habybabady RH, Mohammadi M, Mortazavi SB, Khavanin A, Mirzaei R, Malvajerdi MS. The effect of simultaneous exposure to cigarette smoke and noise on distortion product otoacoustic emissions in rats. Toxicol Ind Health. 2019;35(5):349–57.

    CAS  PubMed  Article  Google Scholar 

  54. Raghuwanshi SK, Gargava A, Kulkarani V, Kumar A. Role of Otoacoustic Emission Test in Neonatal Screening at Tertiary Center. Indian J Otolaryngol Head Neck Surg. 2019;71(Suppl 2):1535–7.

    PubMed  PubMed Central  Article  Google Scholar 

  55. Silva GC, Delecrode CR, Kemp AT, Martins F, Cardoso AC. Transient Evoked and Distortion Product Otoacoustic Emissions in a Group of Neonates. Int Arch Otorhinolaryngol. 2015;19(3):255–8.

    PubMed  PubMed Central  Article  Google Scholar 

  56. Joseph R, Tan HKK, Low KT, Ng PG, Tunnel J, Mathew S. Mass newborn screening for hearing impairment. Southeast Asian J Trop Med Public Health. 2003;34(Suppl 3):229–30.

    PubMed  Google Scholar 

  57. Hunter MF, Kimm L, Cafarlli Dees D, Kennedy CR, Thornton AR. Feasibility of otoacoustic emission detection followed by ABR as a universal neonatal screening test for hearing impairment. Br J Audiol. 1994;28(1):47–51.

    CAS  PubMed  Article  Google Scholar 

  58. Parab SR, Khan MM, Kulkarni S, Ghaisas V, Kulkarni P. Neonatal Screening for Prevalence of Hearing Impairment in Rural Areas. Indian J Otolaryngol Head Neck Surg. 2018;70(3):380–6.

    PubMed  PubMed Central  Article  Google Scholar 

  59. Norton SJ, Gorga MP, Widen JE, Folsom RC, Sininger Y, Cone-Wesson B, Vohr BR, Fletcher KA. Identification of Neonatal Hearing Impairment: Summary and Recommendations. Ear Hear. 2000;21(5):529–35.

    CAS  PubMed  Article  Google Scholar 

  60. Watkin PM. Neonatal screening for hearing impairment. Seminars Neonatol : SN. 2001;6(6):501–9.

    CAS  Article  Google Scholar 

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Acknowledgements

We thank the obstetric medical staff of Hunan Maternal and Child Health Hospital for their cooperation in the investigation.

Funding

This work was finally supported by the Fundamental Research Funds for the Central Universities of Central South University (2020zzts814) and Fundamental Research Funds of Hunan Provincial Health Commission (202112011874).

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Yanying Duan and Xiaoqun Liu conceptualized the investigation. Bingzhi Chen, Lidan Duan, Shaoyi Chen and Muyang Zhang conducted the investigation. Bingzhi Chen drafted the manuscript. Shaoyi Chen and Muyang Zhang participated in the preparation and presentation of the result. The author(s) read and approved the final manuscript. 

Corresponding author

Correspondence to Yanying Duan.

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All the participants signed the written informed consent, which were obtained from their legal guardian, and consented to participate in this investigation. The research protocol and process were approved by the ethics committee of Xiangya School of Public Health, Central South University. All methods used in the present study were performed in accordance with the relevant guidelines and regulations.

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All authors consented for the publication. As the manuscript did not contain information or images that could lead to identification of a study participant, the requirement for specific consent was not applicable.

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The authors declared that they had no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Chen, B., Chen, S., Duan, L. et al. Effects of ambient air pollution, fresh fruit and vegetable intakes as well as maternal psychosocial stress on the outcome of newborn otoacoustic emission hearing screening. BMC Pediatr 22, 269 (2022). https://doi.org/10.1186/s12887-022-03328-9

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Keywords

  • Ambient air pollutant
  • Fresh fruit and vegetable
  • Life event
  • Hearing screening