Disease agents are accumulating in sea life: a wide range of marine animals also contain antibiotic-resistant microbes.

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An unprecedented survey of seabirds, marine mammals, and sharks on the U.S. East Coast has revealed that marine wildlife contains a wide variety of disease-causing microbes--including many that have developed resistance to antibiotics and several that can be transmitted to humans.

The new study provides no evidence that the widespread presence of these disease agents in marine animals is affecting the health of people. But it raises several provocative questions:

* Are more animals acquiring disease-causing microbes in coastal waters increasingly contaminated by human, agricultural, and medical waste?

* Can marine species act as carriers for infectious diseases, spreading pathogens through the oceans?

* Can marine animals that ingest antibiotic-resistant pathogens from medical waste serve as incubators to maintain, multiply, and spread antibiotic-resistant genes through marine and coastal ecosystems?

Over the past four years, a research team led by Woods Hole Oceanographic Institution (WHOI) collected and analyzed samples from 370 marine animals, encompassing 33 species of whales, dolphins, seals, porpoises, sharks, and seabirds, ranging from Kent Island, Canada, to Virginia. WHOI biologists Andrea Bogomolni, Michael Moore, and Rebecca Gast spearheaded the study and led efforts to collect fecal samples from live seals and seabirds, as well as specimens of dead animals found in the wild. The research team necropsied animals in the new Marine Research Facility at WHOI in search of infectious agents.

To collect more specimens, Bogomolni also forged links with stranding networks and fisheries managers, who sent samples of stranded and bycaught animals (animals unintentionally caught in fishing gear) to the WHOI necropsy facility. She accompanied fishermen to gain access to seals on beaches of local islands. She even took advantage of a unique opportunity to collect samples from mako and thresher sharks caught during a local shark-fishing tournament.

The study, published August 2008 in the journal Diseases of Aquatic Organisms, also included Julie Ellis of the Tufts University Cummings School of Veterinary Medicine; Katie Pugliares of International Fund for Animal Welfare Marine Mammal Rescue & Research; and Betty Lentell of the National Marine Fisheries Service.

Giardia, Brucella, and Cryptosporidium 

The researchers focused on testing their specimens for four relatively common microbes known to be zoonotic, or transferable from animals to humans: Brucella, Leptospira, Cryptosporidium, and Giardia, which cause symptoms that include high fever, severe headaches, chills, muscle aches, vomiting, and diarrhea. Thirty-five percent of the animals they examined contained Brucella; 17 percent contained Giardia; 13 percent had Cryptosporidium. To date, initial results indicating the presence of Leptospira in 10 percent of the tested animals have not been confirmed. Altogether, the researchers found nearly 100 types of disease-causing agents in their specimens.

The number of zoonotic agents in the animals surprised the researchers, but they strongly cautioned against interpreting their results as a reason to avoid the beach. Zoonotic microbes are not new, infections usually require a bite or other direct exposure, and people have developed immunities to many such organisms, explained Moore, a WHOI biologist. But it is one of many reasons not to approach beached seals, he said.

Gast, a microbiologist at WHOI, also noted that the presence of Cryptosporidium and Giardia cysts in fecal material does not necessarily mean that the animals were infected; they might be carriers that spread or shed only small amounts of pathogens.

Nevertheless, the presence of Cryptosporidium and Giardia may be an indicator of pollution levels in the ocean, Gast said. The parasites live in the intestines of their warm-blooded hosts and are released to the environment in feces that end up in the ocean.

Marine animals can become infected with zoonotic microbes when they ingest contaminated water while filtering the water for food, or by eating infected prey, such as plankton, shellfish or fish. Some animals--gulls, for example--may become infected by foraging from sewage collection ponds.

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Although Cryptosporidium and Giardia are freshwater inhabitants well-known to wary hikers, these microbes are now popping up in the marine environment, Gast said. People don't drink seawater, but they do consume many of the animals that live in it. Armored with a hard outer shell, the microbes can survive harsh environmental conditions for weeks--more than enough time to be ingested and find a cozy new home inside the gut of an animal or human host.

Reservoirs for antibiotic resistance?

Even more surprising to the researchers was the high number of antibiotic-resistant bacteria harbored in the animals they tested: 73 percent of the animals they tested had at least one type of antibiotic-resistant bacterium; more than 50 percent of the animals sampled had bacteria resistant to two or more antibiotics.

"One porpoise had bacteria with resistance to 15 out of 20 antibiotics we tested for," Bogomolni said. "One of the antibiotics we screened for was gentamicin, which is an agricultural antibiotic. It was ridiculous just looking down the list [of antibiotics] and seeing, 'Resistant, resistant, and resistant.' Porpoises are coastal animals, so maybe they are picking [antibiotic-resistant bacteria] up along their migration."

The finding raises questions about the degree of contamination in coastal waters from treated and untreated sewage discharges or rainwater and river runoff. And it raises concerns that marine animals might act as reservoirs for bacteria--acquiring and maintaining antibiotic-resistant genes and then multiplying and spreading them to other marine life.

"Most of the marine animals sampled have extensive migratory and foraging ranges, and it is likely that they could serve as vectors in the spread of antibiotic resistance in the marine environment," the study's authors wrote.

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"Marine animals interact with each other as predators, scavengers, and through the shared use of marine and beach environments," they wrote. "Our results indicate that marine mammals, fish, and seabirds may not only suffer as victims of disease from zoonotic pathogens, but also act as vectors, moving these human pathogens to different geographic locations in the ocean and terrestrial environments."

Fresh off the boat

The seeds of the study germinated at a Cape Cod Natural History Conference in 2005, when Bogomolni heard a presentation by Becky Harris, Ellis' predecessor as coordinator of SEANET at Tufts University, a program that investigates threats to marine birds throughout the Atlantic coast. Harris described a parasite detected in eider ducks that had died in large numbers recently on Massachusetts beaches (see Page 34). Bogomolni had found the same type of parasite in stranded harp and harbor seals.

About the same time, the National Oceanic and Atmospheric Administration advertised a grant program for research focusing on links between the ocean and human health. Moore, Gast, and Bogomolni applied for funding to begin to investigate zoonotic agents in the marine environment off the U.S. East Coast.

"We wanted to see what was out there and find out what is happening in different populations of animals and what is happening between them," she said.

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Seeking samples of animals to analyze, Bogomolni wrote a letter to officials at the NOAA Fisheries Northeast Observer Program, requesting the delivery to her lab of fresh "bycaught" animals inadvertently caught by fishing boats. The letter resulted in a valuable collaboration, which benefited both Bogomolni and the fishery observer program.

"We received birds sent to us overnight from places like North Carolina and Virginia-that has never happened before," Bogomolni said. "Right off the boat, they came in fresh directly to our door."

"The timing was right," explained study co-author Betty Lentell from the NOAA Fisheries Northeast Observer Program. "Transport wasn't an issue, and we had sufficient staff. We all coordinated and managed the effort to get the samples to the lab so they were as fresh as possible."

The timing was also right because WHOI had just completed building a new Marine Mammal Facility, with a modern suite of necropsy facilities. In a gesture of appreciation for delivering the samples, Bogomolni offered NOAA fisheries observers the opportunity to participate in the necropsies.

Bogomolni had wanted the bycaught animals as a representative sample of "normal" or "healthy" animals, but she discovered that even the bycaught animals were not in good health. The examinations revealed that, similar to the live and stranded animals, bycaught animals also harbored pathogens and antibiotic-resistant microbes. Whether or not the bycaught animals are representative of normal populations requires further research, Moore said.

Sharks and seal poop 

Bogomolni also received support from the Cape Cod Commerical Hook Fishermen's Association, a consortium of fishermen and concerned coastal residents in favor of conserving marine resources through sustainable fishing.

"They arranged to take me out with local fishermen to Chatham Harbor and wait for me while I collected samples with my seal poop collection kit," Bogomolni said. Fecal samples are important in revealing bacteria and parasites.

"The observers and commercial fishermen are now realizing what we can learn from these animals and the importance of collecting data," Bogomolni said.

Greg Skomal, shark research program director at the Massachusetts Division of Marine Fisheries, also assisted in the effort by providing Bogomolni with the opportunity to collect tissue samples from sharks during a shark tournament off Martha's Vineyard.

"It was a bonus opportunity to see what we could learn from these animals that were within the area of our study," Bogomolni explained.

"It's really amazing what you find once you start looking," Bogomolni said. "We've learned that it's not just marine mammals, it's not just birds, and it's not just one geographic area that's affected. You cannot look at a system and just look at one species or one group. Everything is connected."

Samples from bycaught animals were collected under a permit from the NOAA Office of Protected Species.