Low frequency vibrations induce malformations in two aquatic species in a frequency-, waveform-, and direction-specific manner

Although experimental studies of vibration in ovo and in utero did not examine the effects of early exposures, i.e. exposures that correlate to those used in our study where vibrations were applied beginning at the 1-cell stage, they raise an important question: do low frequency vibrations affect human embryonic and fetal development? Embryonic development in aquatic species may be a surrogate to understand similar developmental events in mammals because the mammalian embryo and fetus are localized to an aqueous environment – the amniotic fluid – during development. Furthermore, Xenopus and zebrafish are widely acknowledged to be model organisms to understand the effects of environmental pollutants or as developmental models to understand organogenesis, and studies using these animals provide important knowledge to biomedicine [11], [12], [13], [33], [34], [35], [36]. Thus, if vibrations reach the mammalian womb, they may affect the fetus similar to the effects we have observed in aquatic embryos. Previous studies have shown that sound from the external environment does penetrate the womb [37], and that low frequencies (<200 Hz) change very little as they penetrate the uterus and may even increase inside the womb (reviewed in [38]).

In humans, WBV occurs when vibrations get transferred from a weight-supporting surface to the body [39], [40]. Thus, WBV is an occupational hazard [40], [41] that was estimated to affect 6.8 million US workers (reviewed in [40]), with the highest risks seen in operators of industrial machinery including agricultural machines, construction machines, and transportation vehicles including aircraft, trucks, buses, trains and boats [39], [40], [41], [42]. Epidemiology studies suggest that chronic, long-term exposure to WBV is associated with a variety of health problems [39], [40], [41], [42], [43], with risks that increase with duration of exposure [44]. There is also evidence from epidemiology studies that vibrations can affect human development; studies link exposure to vibration during pregnancy with increased rates of spontaneous miscarriages and stillbirths [45] and others indicate that pregnant women exposed to vibrations in certain occupational settings have an increased risk to have children with central nervous system malformations [46]. Although these epidemiology studies are limited in design, they do indicate a plausible link between low frequency vibrations and birth defects in humans.

Our data indicate that low frequency vibrations cause developmental defects in a species-specific manner. Although heterotaxia and abnormal tail morphogenesis were observed in both zebrafish and Xenopus, neural tube defects were only observed in Xenopus, and isomerisms were observed only in fish. The use of the frog and fish models allowed us to show that low frequency vibrations negatively affect development across species, but our results indicate that the types of vibration that are the most detrimental may differ between species. From these results, we can speculate that low frequency vibrations may affect mammalian development, but this hypothesis requires further testing.

This study characterized the effects of several vibration variables on three distinct biological endpoints. Future studies of frog and fish embryos should characterize the subcellular, cellular and tissue-based targets of vibration that are responsible for the development of neural tube defects and abnormal tail morphogenesis, as well as the critical periods for the effects of low frequency vibrations on these patterning events. In conclusion, we have shown that low frequency vibrations have toxic effects on developing aquatic species, with frequency- waveform- and wave direction-specific effects on three distinct patterning events: neural tube closure, left-right patterning, and tail morphogenesis. Environmental screening is needed to determine whether wildlife populations are exposed to significant amounts of low frequency vibration. Additional experimental and epidemiology studies will shed light on whether humans are affected by these environmental exposures as well.