An important food safety issue in the ocean: silver (Ag) contamination

   Over the past few years, food safety has become an emerging issue due to several food safety scandals, such as the use of gutter oil (recycled oil collected from various sources) and radiation-contaminated foodstuffs. However, the status of food safety for wildlife is still unknown or ignored. Recently, silver nanoparticles (AgNPs) have been extensively used in numerous commercial products, including textiles, cosmetics, and health care items. AgNPs can be released during the production, transport, erosion, washing, and/or disposal of AgNP-containing products, subsequently draining into the aquatic environment and ultimately accumulating in the ocean. Then, Ag can be transferred from one trophic level to the next in the food chain and may exert negative effects on animals at higher trophic levels, such as cetaceans and humans. Therefore, AgNPs are considered potential sources of Ag contamination and have raised public concern about the environmental toxicity of Ag.

   The level of Ag contamination in the environment is expected to increase greatly in the near future, and aquatic animals and marine environments will suffer from the potentially negative impacts of Ag. However, ecotoxicological studies on AgNPs and Ag are still sparse. Cetaceans, as top predators in the ocean, may endure negative health impacts from the long-term deposition of Ag/Ag compounds in their tissues. Most importantly, cetaceans and humans are mammals, and the negative health impacts of Ag/Ag compounds in cetaceans may also affect humans. In other words, cetaceans are sentinel species for the health of marine environments and humans. Hence, it is important to investigate the Ag contamination level in cetaceans. This study retrospectively investigated tissue samples from stranded cetaceans over the last 20 years in Taiwan, developed a histological method (autometallography [AMG]) to evaluate the tissue distribution of Ag, and established a semiquantitative method, a cetacean histological Ag assay (CHAA), to estimate the Ag concentration in cetacean tissues (Figure 1).

   This study was conducted by a collaborative research team from multiple academic units, including Professor Victor Fei Pang, Professor Hui-Wen Chang, Professor Chian-Ren Jeng, Dr. Wen-Ta Li, and Dr. Bang-Yeh Liou at the Graduate Institute of Molecular and Comparative Pathobiology, National Taiwan University (NTU); Professor Wei-Cheng Yang at the School of Veterinary Medicine, NTU; Professor Meng-Hsien Chen at the Department of Oceanography and Asia-Pacific Ocean Research Center, National Sun Yat-sen University; and Professor Hue-Ying Chiou at the Graduate Institute of Veterinary Pathobiology, National Chung Hsing University.

   The present study localized Ag by AMG and developed a model, the CHAA, to estimate the Ag concentrations in liver and kidney tissues from 7 cetacean species. The Ag distribution pattern in cetaceans is different from those observed in previous studies conducted in laboratory rats, and this difference may suggest that cetaceans metabolize Ag differently. Therefore, a presumptive metabolic pathway of Ag in cetaceans is proposed (Figure 2). It is presumed that Ag/Ag compounds can enter the cetacean body via dietary intake and then be delivered to the liver through the gastrointestinal tract and portal circulation. Ag/Ag compounds are considered to be conjugated to proteins during portal circulation. Most of the protein-conjugated Ag/Ag compounds are taken up by hepatocytes, degraded in lysosomes, released into the cytoplasm of hepatocytes, conjugated to proteins, and stored in the lysosomes of hepatocytes. Some Ag/Ag compounds with protein conjugation may remain in blood circulation or may be released from hepatocytes into blood circulation during the renewal of hepatocytes. The Ag/Ag compounds in blood circulation can be subsequently delivered to multiple organs (such as the kidneys), penetrate the glomeruli, and then be reabsorbed by proximal renal tubular epithelium.

   Our study demonstrated that there were no lesions with marked intralesional Ag deposition and no statistically significant correlation between the lesions and Ag concentrations. However, stranded cetaceans are not laboratory animals and are not well controlled in that they are not exposed to only a single contaminant. Therefore, further investigations are warranted to study the systemic Ag distribution, the cause of death/stranding, and the infectious diseases in stranded cetaceans with different Ag concentrations to comprehensively evaluate the negative health effects caused by Ag in cetaceans. Most importantly, this study demonstrated that Ag contamination in cetaceans living in the North Pacific Ocean is more severe than that in other marine regions of the world. The level of Ag deposition in cetaceans living in the former area may have had negative impacts on their health conditions. Furthermore, these 7 cetacean species have different habitats and prey, but the Ag concentration did not significantly differ among the different species. This finding suggests that Ag contamination may exist in all compartments of the marine ecosystem.

Figure 1. Flowchart of the strategy for estimation of the Ag concentration by autometallography (AMG) through a cetacean histological Ag assay (CHAA). (Photo credit: Environmental Pollution, 235, 534-545. DOI: 10.1016/j.envpol.2018.01.010.)

Figure 2. Presumptive metabolic pathway of Ag in cetaceans. Se = selenium; MT = metallothionein; HMWS = high-molecular-weight substances. (Photo credit: Environmental Pollution, 235, 534-545. DOI: 10.1016/j.envpol.2018.01.010.)

Li, W., Chang, H., Chen, M., Chiou, H., Liou, B., Pang, V. F., . . . Jeng, C. (2018). Investigation of silver (Ag) deposition in tissues from stranded cetaceans by autometallography (AMG). Environmental Pollution,235, 534-545. doi:10.1016/j.envpol.2018.01.010.

Dr. Wen-Ta Li
Graduate Institute of Molecular and Comparative Pathobiology

Chian-Ren Jeng
Professor, Graduate Institute of Molecular and Comparative Pathobiology


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