Published online May 23, 2023
Journal of Ecology and Environment (2023) 47:05
1College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University, Chuncheon 24341, Republic of Korea
2Gangwon Wildlife Medical Rescue Center, Chuncheon 24341, Republic of Korea
3Health & Environment Research Institute of Gwangju, Gwangju 61954, Republic of Korea
4College of Veterinary Medicine and Bio-Safety Research Institute, Jeonbuk National University, Iksan 54596, Republic of Korea
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An adult male Eurasian river otter (Lutra lutra) with ataxia and lethargy was rescued. Through the necropsy of this otter with neurological symptoms, a broad range of vascular damage caused by mercury toxicity in several organs, hepatocellular necrosis, and vacuolation in the brain. In mercury examination, liver, kidney, and hair showed values of 0.878 ± 0.027, 1.807 ± 0.049, and 5.712 ± 0.102 μg/g, respectively. Compared with certified reference material, it was confirmed that the concentration of mercury were 6.7 times, 13.7 times, and 43.3 times higher, respectively. When the symptoms and diagnosis results were comprehensively reviewed, this otter’s demise was revealed due to mercury poisoning. The mercury concentration in the liver does not exceed the lowest observed effect level of 3.4 μg/g. However, even at low concentrations, long-term accumulation can cause symptoms including neuropathy, and the possibility that these heavy metals have accumulated in other wild animals cannot be ruled out. It seems that continuous monitoring using sentinel animals is necessary.
Keywords: animal health, Eurasian river otter (Lutra lutra), mercury, public health, wildlife
Mercury (Hg) is a toxic heavy metal that naturally exists as an inorganic or organic compound in the environment (Ebinghaus et al. 1999). Concerns over mercury in the environment developed during the 1950s and 1960s with the poisoning of humans and wildlife in Japan and Sweden. No matter how clean an area is, if there is human activity such as local development, the ecosystems could be contaminated even at very low concentrations when mercury is released (Gworek et al. 2020; Verma et al. 2018), because released mercury is methylated by microorganisms in sediments and converted into highly toxic compounds called methylmercury (MeHg) (Boening 2000; Mergler et al. 2007). MeHg has a much higher bioavailability than normal inorganic mercury and can penetrate cells where there are normally barriers to toxins (Mergler et al. 2007; Ullrich et al. 2001). In other words, it can cross the blood-brain barrier and the placental barrier and directly damage brain and fetal cells. In addition, since bioaccumulation in the food chain occurs as a result of its long half-life and high bioavailability, mercury accumulates in higher concentrations as it moves toward upper predators (Driscoll et al. 2013; Lavoie et al. 2013).
Mercury poisoning causes coma, ataxia, spinal cord degeneration, limb paralysis, tremors, and convulsions and can permanently damage the kidneys, liver, and brain (Boening 2000; Chan et al. 2003). It can also affect the dopamine and cholinergic systems that promote learning and memory, motor function, thermoregulation, and cognition (Basu et al. 2006). In the case of fetuses, spontaneous abortion or fetal cerebral palsy may occur (Chan et al. 2003).
Recently, the anthropogenic emission of mercury has been increasing more rapidly than natural emission, and this is considered a big problem. For example, the amount of mercury measured in Arctic indicator species has increased significantly compared to pre-industrial times (Dietz et al. 2009; Dietz et al. 2011). The international community adopted the Minamata Convention in 2013 to reduce anthropogenic emissions of mercury and thereby prevent damage to people and ecosystems caused by mercury, and the convention came into force in 2017 (Kessler 2013; Science for Environment Policy 2017).
Sentinel animals are widely used as an environmental indicator species when monitoring pollutants. Predatory apex predators in river such as otters and minks are commonly used as sentinel species for risk assessment in freshwater ecosystems (Baos et al. 2022; Basu et al. 2007). Unlike birds, they have a small range and do not hibernate or migrate, so they are exposed to pollutants year-round (Hung and Law 2016). Biomarkers of exposure, such as tissue concentrations, can be used to determine environmental concentrations using sentinel species and enable assessment of the risk posed to humans (Peterson and Schulte 2016).
Hwacheon-gun, South Korea, is nicknamed the city of water for its clean environment. The freshwater ecosystem is well preserved and inhabited by many Eurasian river otters, and it is a place with varied natural scenery. One Eurasian river otter found in this clean area was unable to control its body, and it was rescued but died soon after. Various examinations, including necropsy, were performed. The cause of death was revealed as mercury poisoning.
An adult male Eurasian river otter (
As a routine treatment for this kind of case, 10 mg/kg cefazolin sodium (Cefazolin Inj.; Chong Kun Dang Pharmaceutical Corp., Seoul, Korea), 0.5 mg/kg famotidine (Gaster Inj.; Dong-A ST, Seoul, Korea), 2 mg/kg ornipural solution (Vetoquinol, Magny-Vernois, France), 6 mg/kg aminoethyl sulfonic acid (Taurine-F Inj.; Samyang Anipharm Co., Ltd., Seoul, Korea) and 1 mg/kg L-Ornithine-L-Aspartate (Hepa-Merz Infusion; Hanwha Pharma Co., Ltd., Seoul, Korea) were intravenously injected.
There was no recovery from this condition, and the otter died at 4 days post rescue and was then subjected to postmortem examination. During necropsy, representative tissue samples were collected in 10% neutral buffered formalin for histopathological examination or placed in a deep freezer (–80°C) for further additional examination, if necessary.
Blood tests and radiological examination for neurological signs, ataxia, and spinning movement were performed for detailed diagnosis. The Eurasian river otter was anesthetized in sternal recumbency with 2.5 mg/kg alfaxalone (Alfaxan®; Jurox Inc., North Kansas City, MO, USA), maintained with isoflurane inhalation, followed by the computed tomography (CT) scanning using a Somatom Emotion 6 (Siemens, Erlangen, Germany) and magnetic resonance imaging (MRI) using a Vantage Elan (Toshiba, Tokyo, Japan).
Tissue samples were fixed in 10% (w/v) neutral formalin for 24–48 hours and routinely processed as described elsewhere (Cho et al. 2023). Briefly, formalin-fixed tissue samples were trimmed, dehydrated in a series of graded ethanol solutions, cleared in xylene, and embedded in paraffin blocks. Sections of 4
The total mercury levels were measured in the liver, kidneys and fur using a DMA-80 Direct Hg Analyzer (Milestone, Sorisole, Italy). The analytical quality was controlled using procedural blanks, triplicates and BCR®-277R Estuarine Sediment (Institute for Reference Materials and Measurements [IRMM], Geel, Belgium) as certified reference material (CRM).
Complete blood counts showed elevations in white blood cells, neutrophils, monocytes (MON), mean corpuscular volume, mean corpuscular hemoglobin and a decrease in lymphocyte (Table 1). Serum chemistry analysis revealed elevations in alkaline phosphatase, alanine aminotransferase and a decrease in amylase (Table 1). The results are suggestive of anemia, chronic hepatitis, pancreatitis, and inflammation-like immunomodulation.
In CT and MRI, chronic hemorrhage was observed in the meninges and brain parenchyma (Fig. 1).
After conducting a gross pathological examination, no abnormalities were observed in the external appearance except for severe emaciation (Fig. 2).
At postmortem examination, severe meningeal hemorrhage and edema was observed in the brain (Fig. 3). Diffuse hemorrhage of lungs, left ventricular hypertrophy of heart, and enlarged auxiliary lymph nodes were observed. Hyperemia, erosion, ulceration, and bleeding were observed in the stomach.
Microscopically, diffuse sinusoidal dilation and hepatocellular necrosis in the liver (Fig. 4A), and myocardial focal necrosis in heart (Fig. 4B) were found. Diffuse congestion and/or hemorrhage and edema were observed in lungs. In particular, infiltration of inflammatory cells around the capillaries and vascular edema was seen in the right cerebrum and multifocal edema was observed in the cornu ammonis 2 region and molecular layer (Fig. 4C).
The mercury concentrations in the liver, kidney and fur were 0.878 ± 0.027, 1.807 ± 0.049, and 5.712 ± 0.102
Mercury poisoning can cause various gross pathological changes in the affected individual. One of the common findings is central nervous system (CNS) damage, as seen in our case. Mercury has a strong affinity for nervous tissue, and chronic exposure can cause damage to the CNS. Gross pathological changes in the brain may include atrophy, focal necrosis, and edema (Takahashi and Shimohata 2019). Other lesions include interstitial nephritis, tubular necrosis and glomerular damage in the kidney; hyperemia, erosions, and ulcers in the stomach and intestines; interstitial congestion and fibrosis, emphysema, and bronchitis in the lungs. In the case of pulmonary damage, this may be due to inhalation of mercury vapors, which can cause damage to the lungs (Raffee et al. 2021). Mercury toxicity can also affect the cardiovascular system, causing damage to the heart muscle and blood vessels. Myocardial necrosis, endocarditis, and vasculitis were seen in our case (Omanwar and Fahim 2015).
Initially, the attribution of the Eurasian river otter’s demise to mercury poisoning did not appear tenable, given the location of its discovery in a protected otter habitat that was deemed environmentally pristine. However, the surrounding environs had undergone significant developmental activity, including the recent establishment of a waste disposal site and a golf course, prompting doubts about the ecological integrity of the area.
Lesions consistent with mercury poisoning include CNS damage, renal necrosis and fibrosis, vascular damage, and liver damage. Renal necrosis and fibrosis have been reported in several experimentally administered species, including otters, mink, and human (Farina et al. 2011; Heinz 1996). The cause of these pathological changes in the kidney is thought to be autoimmune glomerulopathy due to chronic inorganic mercury filtration (Eto et al. 1997; Gao et al. 2022). In the case of liver damage, mercury oxidative stress is known to induce liver necrosis and sinusoid dilation (Balali-Mood et al. 2021; Yahyazedeh et al. 2017). In neurological symptoms, MeHg-induced excitotoxicity and demyelination due to oxidative stress are the main causes (Fernandes Azevedo et al. 2012). Moreover, vascular damage is also caused by MeHg-induced oxidative stress, which further accelerates damage to other organs (Takahashi and Shimohata 2019).
Humans, wildlife, and the environment are organically linked as part of the “One Health” concept. Obtaining information on mercury exposure in wildlife, especially sentinel animals such as river otters can provide insight into risks to the environment and humans. Various countries, such as Denmark and the United States, are already conducting monitoring of pollutants using sentinel species, and research on models is also being actively conducted (Dibbern et al 2021; Fusillo et al. 2022; Yates et al. 2005).
The mercury concentration was recorded in as 1.807 ± 0.049
Through the necropsy of an adult male Eurasian river otter (
This suggests that even in clean areas with low concentrations of environmental pollutants, toxic symptoms can be caused by the continuous accumulation of pollutants. Therefore, it cannot be ruled out that other wild animals may also accumulate pollutants such as heavy metals. It is important to measure concentrations of pollutants in the environment, but it will also be important to evaluate the extent to which pollutants have accumulated in the body using sentinel animals.
CRM: Certified reference material.
CT: Computed tomography.
MRI: Magnetic resonance imaging.
H&E: Hematoxylin and eosin.
IRMM: Institute for Reference Materials and Measurements.
CNS: Central nervous system.
KGR and SJA collected and analyzed data, wrote original draft. SJL, SYC, and BRDK collected data. HSC conceptualized and supervised the research, and reviewed the draft. YO acquired the research grant and conceptualized and supervised the research, and reviewed and edited the draft. The authors read and approved the final manuscript.
This work was supported by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through Animal Disease Management Technology Advancement Support Program, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (Project No. 122013-2).
All data generated or analyzed during this study are included in this published article.
The authors declare that they have no competing interests.