Fish swim slower if parents exposed to flame retardant.

Jan 29, 2013

Chen, L, K Yu, C Huang, L Yu, B Zhu, PKS Lam, JCW Lam and B Zhou. 2012. Prenatal transfer of polybrominated diphenyl ethers (PBDEs) results in developmental neurotoxicity in zebrafish larvae. Environmental Science & Technology http://dx.doi.org/10.1021/es302119g.



Synopsis by Craig Butt and Wendy Hessler

2012-1220zebrafish
Novartis AG/flickr

Young zebrafish exposed to flame retardants through their mothers swam up to 60 percent slower and had reduced gene expression important for nervous system development. In natural settings, slower swimmers are easier targets for predators. A new study is unique because it shows in fish that exposure to PBDEs, found in some furniture and electronics, can lead to developmental and behavioral changes in their offspring. Researchers use zebrafish to better understand how exposure to pollutants during development can affect the nervous system of vertebrates.

 


Context

The central nervous system is very sensitive to harmful chemicals, especially during early life (Rice and Barone 2000). Damage to brain cells during early development can negatively affect brain functions and behavior in later life. Often these effects are subtle and difficult to detect.

Researchers commonly use zebrafish to study how environmental contaminants harm the brain (Hill et al. 2005, Linney et al. 2004). The fish are good models because their nervous system is very similar in structure and function to humans and other mammals.

Polybrominated diphenyl ethers (PBDEs) are a large group of chemicals mainly used as flame retardants. They are commonly added to furniture foams, plastics, textiles and electronics to slow burning during fires.

PBDEs were produced in three types of mixtures known as pentaBDE, octaBDE and decaBDE. These mixtures have different amounts of bromine atoms attached to their carbon backbone. PentaBDE was mainly used in foams, such as those used in furniture.

Over time, PBDEs are released from the foams and other parts of the products. The flame retardants are commonly detected in indoor air and house dust (Stapleton et al. 2012).

They also are measured in human blood, urine, breast milk and placental cord blood (Sjödin et al. 2008, Jakobsson et al. 2012). PBDEs, then, can pass from a mother to her developing fetus and nursing infant. Egg-laying animals, such as fish, pass the chemicals into their eggs.

PBDEs have been linked to liver and thyroid toxicity, as well as neurodevelopment toxicity. Limited studies suggest effects on cognition and behavior in children (Herbstman et al. 2010). Because of these health effects, the pentaBDE and octaBDE mixtures were banned throughout most of the world. The decaBDE mixtures are scheduled for phase-out in 2013.

Even so, because they are long-lived, PBDEs still are widely detected in the environment, in wildlife and in people (de Wit et al. 2010).

What did they do?

Male and female adult zebrafish were exposed to one of three concentrations of a pentaBDE mixture known as DE71 through their water. PentaBDE contains mostly PBDEs with four and five bromine atoms attached to its carbon backbone.

The fish were exposed to 0.16, 0.8 or 4.0 μg/L of the DE71 for 150 days. Some fish were put into clean water for comparison.

After the exposure period, the researchers bred the fish, collected the eggs and measured PBDE levels in the eggs to determine the amount transferred from the parents.

The eggs were placed in clean water and hatched. At 4 days old, the larvae's swimming speed was measured in an alternating dark–light–dark system that simulated day and night. Deviations from unexposed fish would indicate a neurodevelopment effect.

The researchers measured the expression of several genes and proteins important for nervous system development. Also, they measured acetylcholinesterase (AChE) activity and protein levels in the fish brains. AChE is an enzyme that stops signal transmission between neurons and is important for normal nervous system function.

What did they find?

The adult zebrafish that swam in the pentaBDE-contaminated water accumulated the flame retardant chemicals in their bodies. During reproduction, the mothers transferred some of the chemicals to their eggs.

The fish exposed to higher pentaBDE levels in the water had higher levels in their bodies and higher levels in the eggs.

Swimming behavior in the exposed larvae slowed and differed between light and dark periods. The larvae of the pentaBDE exposed parents swam up to 35 percent slower during the dark period and up to 64 percent slower during the light period. In the dark periods, higher levels of PBDE exposure resulted in slower-swimming babies.

Also, expression of three genes that are critical for normal brain and neurological development was reduced. At the highest dose tested, expression fell 1.7 times. Further, the levels of proteins made by two of the affected genes were reduced by up to 33 percent and 58 percent.

The zebrafish larvae also had reduced AChE gene expression – up to 37 percent in the highest-exposed fish. In addition, activity levels of the AChE enzyme were up to 29 percent lower in the pentaBDE-exposed larvae.

What does it mean?

The study is one of the first to show, in fish, that PBDE exposure to parents can lead to altered brain and nervous system development in their offspring. Such early life changes to the neurological system can lead to learning and behavioral problems later in life.

Zebrafish often are used to study how environmental contaminants affect the brain because their nervous systems are very similar to humans and other mammals. In addition, the fish develop faster and are easier to care for as compared to rodents and other animals typically used to study neurodevelopment.

The results are unique because the zebrafish larvae were exposed to the PBDEs through their parents. The pentaBDE chemicals accumulated in the exposed parents during the five-month exposure time, and the mothers transferred some of these chemicals into their eggs.

Three different target measures showed the pentaBDE mixture affected the offspring's development. First, the chemicals were passed from the parents to the offspring via the eggs. This was not surprising since it is known that many persistent chemicals can pass from the mother to the fetus or eggs.

Second, behavior changes were documented in the larvae. The offspring of the pentaBDE-exposed parents swam slower during both light and dark. But, with the exception of the swimming effects, the fish appeared to be otherwise healthy.

Third, enzyme and gene activity as well as protein levels associated with nervous system development were reduced. Three genes necessary for proper neurological development were impaired by the pentaBDE exposure. This finding provides some insight into how the brain was damaged. In addition, levels of AChE gene expression and enzyme activity were reduced in the pentaBDE-exposed fish. AChE is necessary for the proper signal transmission in neurons.

This research contributes to an increasing number of studies that shows early life exposure to PBDEs can impact locomotion. Previous studies have found that zebrafish embryos exposed to the pentaBDE mixture – or one of its main chemical components (BDE 47) – swim slower as larvae (Chen et al. 2012a, Chen et al 2012b) during similar light-dark tests.

But in a similar study in which the parents were exposed to the decaBDE flame retardant mixture, larvae actually swam faster during the light and dark tests (He et al. 2011). Although this suggests that locomotion behavior may be a common target for different PBDEs, the actual effect may vary.

These findings have direct implications for predator-prey avoidance in fish, but also have implications for humans and other mammals. This is because scientists use these types of locomotion tests as a measure of how individuals interact with their surrounding environment. Impaired environmental interaction is characteristic of behavioral impacts such as ADHD.

In the study, the fish were subjected to alternating dark-light cycles. Under normal conditions when switching from light to dark conditions, fish will initially swim faster and then gradually slow down. The slower swimming speed in the pentaBDE-exposed fish may indicate that they did not respond as quickly to the changes in light conditions. This may indicate a reduced ability to interpret changes in their environment.

The scientists do not know the way the pentaBDE chemicals damaged the brain, but they think it may be related to the thyroid hormone system. Thyroid hormones are essential for proper brain development, and it is well known that PBDEs can disrupt thyroid hormones.

The study investigated a commercial flame retardant mixture, called pentaBDE. This mixture is now banned, but the chemicals that are in the penta-BDE mixture are still widely detected in the environment, including house dust (Stapleton et al. 2012).

A limitation of the study is that the fish were exposed to very high levels of PBDEs, about 1,000 times higher than typical environmental levels (Oros et al. 2005). It is not known if similar effects would have been observed with lower, environmentally relevant PBDE levels.

Future work should examine if the effects on swimming persist through the fish's life. Also, additional work should investigate if the harmful effects are transferred to future generations, such as the grandchildren.

Resources

Chen, L, C Huang, C Hu, K Yu, L Yang and B Zhou. 2012a. Acute exposure to DE-71: Effects on locomotor behavior and developmental neurotoxicity in zebrafish larvae. Environmental Toxicology and Chemistry 31(10):2338-2344.

Chen, XJ, CJ Huang, XC Wang, JF Chen, CL Bai, YH Chen, XP Chen, QX Dong and DR Yang. 2012b.  BDE-47 disrupts axonal growth and motor behavior in developing zebrafish. Aquatic Toxicology 12:35-44.

de Wit, CA, D Herzke and K Vorkamp. 2010. Brominated flame retardants in the Arctic environment - trends and new candidates. Science of the Total Environment, 408(15):2885-2918.

He, J, D Yang, C Wang, W Liu, J Liao, T Xu, CL Bai, JF Chen, KF Lin, CH Huang and QX Dong. 2011. Chronic zebrafish low dose decabrominated diphenyl ether (BDE-209) exposure affected parental gonad development and locomotion in F1 offspring. Ecotoxicology 20(8):1813-1822.

Herbstman, JB, A Sjödin, M Kurzon, SA Lederman, RS Jones, V Rauh, LL Needham, D Tang, M Niedzwiecki, RY Wang and F Perera. 2010. Prenatal exposure to PBDEs and neurodevelopment.  Environmental Health Perspectives 118(5):712-719.

Hill, AJ, H Teraoka, W Heideman and RE Peterson. 2005. Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicological Sciences 86(1):6-19.

Jakobsson, K, J Fang, M Athanasiadou, A Rignell-Hydbom and A Bergman. 2012. Polybrominated diphenyl ethers in maternal serum, umbilical cord serum, colostrum and mature breast milk. Environment International 47:121-130.

Linney, E, L Upchurch and S Donerly. 2004. Zebrafish as a neurotoxicological model. Neurotoxicology and Teratology 26(6):709-718.

Oros, RD, D Hoover, F Rodigari, D Crane and J Sericano. 2005. Levels and distribution of polybrominated diphenyl ethers in water, surface sediments, and bivalves from the San Francisco estuary. Environmental Science & Technology 39(1):33-41.

Rice, D and S Barone. 2000. Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environmental Health Perspectives 108(Supplement 3):511-533.

Sjödin, A, LT Wong, RS Jones, A Park, Y Zhang, C Hodge, E Dipietro, C McClure, W Turner, LL Needham and DG Patterson Jr.  Serum concentrations of polybrominated diphenyl ethers (PBDEs) and polybrominated biphenyl (PBB) in the United States population: 2003-2004. Environmental Science and Technology 42(4):1377-1384.

Stapleton, HM, S Eagle, A Sjödin and TF Webster. 2012. Serum PBDEs in a North Carolina toddler cohort: Associations with handwipes, house dust, and socioeconomic variables.  Environmental Health Perspectives 120(7):1049-1054

 

 

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