Gestational exposure to polychlorinated biphenyls and dibenzofurans induced asymmetric hearing loss: Yucheng children study

Highlights

• Yucheng cohort has been exposed to high doses of dioxin-like chemicals.

• We examined hearing function in children born to Yucheng women.

• Mild hearing loss was found in Yucheng children's early adulthood.

• Such damage was related to gestational exposure to 2,3,4,7,8-pnCDF.

Abstract

Introduction

In 1979, approximately 2000 people in central Taiwan were exposed to polychlorinated biphenyls and dibenzofurans (PCBs/PCDFs) due to ingestion of contaminated rice oil. The children born to mothers exposed to PCBs/PCDFs were called Yucheng children. We conducted a follow-up study to examine the association between gestational PCBs/PCDFS exposure and auditory function in Yucheng children's early adulthood.

Methods

In 1985 and early 1992, Yucheng children and their age, gender, socio-economic matched unexposed referent children were recruited for physical examination and long-term follow-ups. In 2007, Yucheng children and referent children were invited to participate in a health examination, including assessment of pure-tone air-conduction thresholds and distortion product otoacoustic emissions (DPOAEs) test. Gestational exposure to PCBs/PCDFs in Yucheng children were estimated by back-extrapolation of their mother's serum concentration to the time of childbirth.

Results

A total of 86 Yucheng children (51.2% males) and 97 referent children (50.5% males) were included for analysis. No difference was found in demographic characteristics between two groups. Among the Yucheng children, 53 had estimated PCBs/PCDFs concentrations. We found that Yucheng children were at higher risk of having elevated hearing threshold at low frequencies in the right ear. Estimated maternal concentrations of 2,3,4,7,8-pnCDF at the time of birth were associated with increased hearing thresholds and decreased DPOAEs amplitudes at low frequencies in the right ear.

Conclusion

Gestational exposure to PCBs/PCDFs caused adverse asymmetrical hearing effects detectable even in early adulthood.

Introduction

Polychlorinated dibenzodioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and polychlorinated biphenyls (PCBs) are widespread environmental pollutants. The use of these chemicals are currently banned or restricted in most developed countries. However, because of the chemicals' persistence in the environment, high background concentrations are still found as seen in several large-scale epidemiologic studies in the general population (Patterson et al., 2008, Patterson et al., 2009, Wong et al., 2008). Due to the world-wide ubiquitous background exposure, PCDDs, PCDFs, and PCBs are still a concern to human health. PCBs have been suggested as neurotoxicants especially when exposed during prenatal and early postnatal periods, and known to cause neurological effects including neurocognitive deficits, behavioral problems, and auditory impairments (Boucher et al., 2010, Grandjean and Landrigan, 2006, Schantz, 1996, Schantz et al., 2003, Tilson et al., 1998). We and others have reported neurological adverse effects in the children prenatally exposed to PCBs and PCDFs (Chen et al., 1992; Jacobson and Jacobson, 1996; Lin et al., 2008).

Several animal studies have demonstrated auditory deficits after gestational PCB exposure. In rats, gestational exposure to a commercial PCB mixture, Aroclor 1254, resulted in low-frequency hearing loss (Goldey et al., 1995, Lasky et al., 2002). The rats with gestational exposure to a mixture of 35% Aroclor 1242, 35% Aroclor 1248, 15% Aroclor 1254, and 15% Aroclor 1260 had decreased hearing function as measured by an objective method, distortion product otoacoustic emissions (DPOAE), including reduced amplitudes and elevated thresholds across a wide range of frequencies (Powers et al., 2009, Powers et al., 2006). More recently, a study suggested an additive effect of PCBs and polybrominated diphenyl ethers (PBDEs) on cochlear function, evidenced by reduced DPOAE amplitudes and increased DPOAE thresholds in rats (Poon et al., 2011).

Further investigation on the auditory pathway showed that rats exposed to Aroclor 1254 decreased amplitude of the early brainstem auditory evoked response (BAER) peaks, a measurement for the damage in the brainstem auditory pathways (Herr et al., 1996). The authors suggested that the deficit might exist at the level of the cochlea and/or auditory nerve. A recent study in rats confirmed PCB-52 and PCB-180 effect on elevation BAER threshold. This study also indicated that different PCB congeners had varied potencies, as PCB-52 had greater effect on BAER threshold than PCB-180 (Lilienthal et al., 2011).

In humans, studies on auditory effects of gestational exposure to PCBs are limited. A study in 7-year-old children in Faroe Islands found a positive association between prenatal PCB exposure and auditory thresholds at frequencies 250 and 12,000 Hz in only the left ear (Grandjean et al., 2001). In a follow-up study of mother-child pairs in 12 U.S. centers, higher PCB concentration in maternal serum was related to increased hearing thresholds at 2000 Hz in the left ear, and 4000 Hz in the right ear when the children were 8 years of age (Longnecker et al., 2004). Swedish boys, born to fishermen's wives and sisters in east coast, who were exposed to organochlorine, according to plasma PCBs concentrations (Grimvall et al., 1997, Rylander et al., 1997), had higher prevalence of hearing loss as compared to boys born to fisherman families in west coast, where exposure to PCBs was low. However, somehow conflicting results were also found, that the boys from fisherman's families of east coast did not have poorer hearing ability as compared to the local reference population, who were not highly exposed to PCBs (Rylander and Hagmar 2000).

In 1978–1979, an episode of mass exposure to toxic agents occurred in central Taiwan. Approximately 2000 victims ingested rice oil contaminated with PCBs (Kanechlor-500) and their pyrolytic products (Hsu et al., 1985). After an average of 9–10 months of exposure, the etiology was confirmed by health authority that one specific brand of rice oil was contaminated and was the causal agent of this mass poisoning. Repeated heating of the PCBs resulted in generation of PCDFs and polychlorinated quaterphenyls (PCQs). Based on the interviews with 98 Yucheng patients, average consumption was estimated to be 1 g (range=0.7–1.4) of PCBs and 3.8 mg (range=1.8–5.6) of PCDFs (Lan et al., 1981), averagely. More than 13 years after the Yucheng incident, Yucheng mothers continued to have detectable serum concentrations of PCB/PCDF congeners that were many times higher than that of the unexposed controls (Guo et al., 1997). The children born to mothers exposed to PCBs and related compounds were called Yucheng children. Our previous study showed that Yucheng children had a higher incidence of otitis media than referent children (Chao et al., 1997). No auditory assessment was performed during that time. We therefore conducted a follow-up study to test the hypothesis whether children prenatally exposed to PCBs and PCDFs had higher risk of developing auditory deficits, as compared to their referent children. We also examined whether hearing effects were associated with gestational PCBs/PCDFS exposure or exposure to specific congeners in the Yucheng children.