Animal sentinels sounding the alert

From ocean health to fracking's impact, animals are trying to tell us something. Are we listening?​

Veterinarians are accustomed to protecting animal health, but in some instances, animals end up protecting human health.

Several characteristics contribute to the ability of pets to serve as sentinels for human diseases. They are less mobile than humans and constantly exploring their environment by smelling and licking objects. Especially if they are small, they may be more sensitive than humans to a fixed dose of a toxin or infectious agent. And, generally, they have a shorter latency for most toxic events.

Today, some researchers are relying on sentinel species to study the biological effects of toxic materials and chemicals. By measuring these effects with the sentinel species in its natural habitat, researchers have the opportunity to evaluate several factors, including the effects of certain chemical combinations, of graduated exposure, and of low-level exposure over extended periods of time.

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​	​An Atlantic bottlenose dolphin is lifted off the boat and back into the water following a health examination. Routine examinations are performed as part of the Atlantic Bottlenose Dolphin Health and Environmental Risk Assessment Project to help scientists and researchers better understand the dolphins' health in the context of their ecosystem. (Photos by Georgia Aquarium/Addison Hill)	​

Reports of reproductive problems in animal populations, including developmental abnormalities and behavioral disturbances, have prompted concerns that chemical exposures could be affecting both animals and humans. The same goes for climate change. Although the evidence linking animal disease events to human health is currently limited, such links represent an emerging field of study that is being led by veterinary researchers.

Swimming with the dolphins

Dr. Gregory Bossart, senior vice president and chief veterinary officer at the Georgia Aquarium, has focused his research on marine mammals as sentinel species for ocean and human health. He has found that marine mammals are prime sentinel species because many have long lifespans, are long-term coastal residents, feed at a high trophic level, and have unique fat stores that can serve as depots for anthropogenic toxins. Marine mammals may be exposed to environmental stressors such as chemical pollutants, harmful algal biotoxins, and emerging or resurging pathogens. Because many marine mammal species share the coastal environment with humans and consume the same food, they also may serve as effective sentinels for public health problems.

To further investigate, Dr. Bossart and his colleagues started the Atlantic Bottlenose Dolphin Health and Environmental Risk Assessment Project in 2003 when he was director of the Marine Mammal Research and Conservation Program at Florida Atlantic University. A multidisciplinary and multi-institutional cooperative effort, HERA was designed to evaluate the individual and population health of bottlenose dolphins in two southeastern U.S. coastal regions: Charleston, South Carolina, and the Indian River Lagoon, Florida, which is part of the longest barrier island complex in the United States, occupying more than 30 percent of Florida's eastern coast.

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​	​Dr. Gregory Bossart checks for respiratory health as part of an examination on a wild dolphin during a 2015 health and environmental risk assessment project.	​

"The beauty of the study is the Indian River Lagoon is 180 miles long. The dolphins don't leave the area often, so what is impacting the area environmentally will more effectively impact this population. We've been able to follow their health and disease over a period since 2003, so we have been able to follow these trends," Dr. Bossart said.

"What was interesting in the 360 dolphins studied was we found various infectious and noninfectious diseases that parallel emerging public health and environmental issues."

In particular, the Indian River Lagoon has drastically changed, from changes in salinity and pH concentrations to changes in temperature, he said, resulting in algal blooms and a massive die-off of seagrasses, which impacts ecosystem and animal health. The changes also have encouraged the emergence of diseases that previously were unrecorded in this study area, Dr. Bossart said.

The HERA research team has documented a variety of infectious disease agents such as dolphin morbillivirus as well as emerging papillomaviruses and herpesviruses associated with orogenital tumors, not to mention chlamydia, new fungal organisms, and other pathogens.

The clearest example, though, of dolphins as sentinels occurred when the HERA research team found that the dolphins had some of the highest concentrations of mercury ever found in marine mammals. Taking this information, they looked at coastal human populations—specifically fishermen in the area—and found they, too, had high concentrations of mercury. Currently, Dr. Bossart and the HERA research team are looking at pregnant women in the area and testing for mercury exposure to see how important a public health issue this might be.

"Sentinel species are an important component of the one-health initiative, and veterinarians are becoming a key component of that because of their unique training," Dr. Bossart said.

"They're trying to tell us what's going on in our oceans, and we're not good at listening to that. It's important for us to look into that, from an infectious disease standpoint. Three-quarters of infectious diseases in humans are zoonotic. We have our work cut out for us. In our place, we need to pay attention to what dolphins are telling us about their health and the health of oceans."

HERA researchers and Georgia Aquarium plan to expand the geography of the study into northern Florida. They currently examine stranded marine mammals around the St. Augustine area and have found high concentrations of infectious diseases in stranded animals there, Dr. Bossart said. They plan to compare the values in that population with those of the Indian River Lagoon dolphins.

Canary Database

As research into animals as sentinels continues, a database has been created to index thousands of peer-reviewed scientific studies that give evidence of animals as early warning monitors of human health hazards.

Peter Rabinowitz, MD, associate professor in the Department of Environmental and Occupational Health Sciences at the University of Washington School of Health, directs the Center for One Health Research. As part of that, he created the Canary Database (http://canarydatabase.org), an online resource providing evidence of animals as sentinels of environmental health threats from both toxic and infectious hazards. The database includes studies of wildlife, companion animals, and livestock in which either the exposure or the health effect is potentially relevant to human health. For each study, curators add information about animal species, exposures, health effects, location, and whether the study includes data linking animal sentinel events to human health risks in the following ways:

• Exposure-effect relationships in the animal.
• Shared exposures between human and nonhuman animals.
• Interspecies susceptibility.
• Linkage between animal and human health outcomes.
• Gene sequence information.
• Suggested uses of the data.

The goal is to develop ways to better understand and use animal and human disease sentinel events to detect and control shared health threats from biological, chemical, and physical hazards in the environment.

Dr. Rabinowitz and others have been investigating the impact fracking has on humans and animals, for example. Natural gas extraction activities, including the use of horizontal drilling and hydraulic fracturing, may pose health risks to both human and animal populations in close proximity to sites of extraction activity.

In a study published in March 2015 in the Journal of Environmental Science and Health, researchers (including Dr. Rabinowitz) hypothesized that because animals may have increased exposure to contaminated water and air as well as more susceptibility than nearby humans to contaminant exposures, animal disease events in communities living near natural gas extraction may provide sentinel information useful for human health risk assessment.

They collected health data on 2,452 companion and backyard animals living in 157 randomly selected households of Washington County, Pennsylvania, which is an area of active natural gas drilling. A total of 127 health conditions were reported, most commonly among dogs. When reports from all animals were considered, no meaningful associations were found between reported health conditions and household proximity to natural gas wells. When data on dogs were analyzed separately, the researchers found an increased risk of "any" reported health condition in households less than 1 kilometer from the nearest gas well, with skin conditions being the most common.

Not surprisingly, many of these same researchers did a follow-up study based on the self-reported health symptoms of nearly 500 people in 180 households in the same area. The results of this one, published in the January 2018 issue of Environmental Health Perspectives, showed that even when accounting for confounding variables, such as age, cigarette smoking, education level, and occupation, residents who lived less than 1 kilometer from a gas well reported more health symptoms than those living more than 2 kilometers from a gas well.

Residents living less than 1 kilometer from a gas well were also more likely to report skin conditions during the previous year as well as upper respiratory tract symptoms. Even after adjusting for other health risk factors, such as smoking, household proximity to natural gas wells was associated with increased health conditions.

The study did not find an association between proximity to a natural gas well and increased cardiac, neurologic, or gastrointestinal symptoms.