Land-to-sea Transmission of Toxoplasmosis ... And Back Again
ASTM Conference Coverage
By Mary-Louise Scully, MD
Dr. Scully is Director, Travel and Tropical Medicine Center, Sansum Clinic, Santa Barbara, CA.
Dr. Scully reports no financial relationships relevant to this field of study. This study originally appeared in the February issue of Travel Medicine Advisor. It was edited by Frank Bia, MD, MPH, and peer reviewed by Mary-Louise Scully, MD. Dr. Bia is Professor (Emeritus) of Internal Medicine (Infectious Disease and Clinical Microbiology), Yale University School of Medicine, and Dr. Scully is Director, Travel and Tropical Medicine Center, SansumClinic, Santa Barbara, CA.; they both report no financial relationships relevant to this field of study.
At the recent 58th annual meeting of American Society of Tropical Medicine and Hygiene held in Washington D.C., Dr. Patricia Conrad of the University of California, Davis School of Veterinary Medicine, provided an excellent presentation during the Scientific Session on Protozoa entitled "Tracking Toxoplasma gondii from Land to Sea." Conrad and her colleagues have been exploring the complex relationship between marine and terrestrial environments in toxoplasmosis transmission to California sea otters. Their research shows that the increasing prevalence of toxoplasmosis in California sea otters is linked to coastal fresh water runoff of infective Toxoplasma gondii (T. gondii) oocysts from cat feces, both domestic and feral. These findings are especially noteworthy in that a recent study found ingestion of raw or undercooked clams, oysters, and mussels to be an emerging risk factor for human toxoplasmosis acquisition as well.1
Sea otters were once abundant along the Pacific Rim, but these animals were hunted to near extinction for their soft, dense, highly valued fur, often referred to as "soft gold" among hunters. In 1911, sea otter hunting was finally banned under an international treaty signed by Russia, Japan, Great Britain, and the United States. Under legal protection, some sea otter populations in Alaska and the Pacific Northwest have rebounded. However, the California southern sea otter (Enhydra lutris nereis) has struggled, and remains listed as a threatened species, numbering only about 2,800. The causes for their decline are likely multi-factorial, but a partial explanation is parasitic infections such as T. gondii and Sarcocystis neurona.
T. gondii can infect a wide variety of animals, but domestic and wild felids (felines) are the only definitive hosts where sexual multiplication of the results in formation of oocysts that are passed in the feces, sporulate in the environment, and are infective to susceptible hosts. Cats are infected by eating tissue cysts of infected birds or rodents or by eating sporulated cysts from other cats. Under laboratory conditions, cats can shed as many as 500 million oocysts, and they may shed oocysts for up to 20 days. The natural instinct of cats to bury their feces and defecate in shaded areas can allow the cysts to remain infective for as long as 18 months.2 These infective oocysts in soil may then be transported into freshwater and marine waters via sewage, storm, and freshwater runoff.
It is known that T. gondii can cause fatal encephalitis in California sea otters. Conrad and colleagues studied 223 live and dead sea otters between 1997 and 2001 and found a seroprevalence rate of 42% (49/116) for live otters and 62% (66/107) for dead otters. Importantly, they found that otters sampled near coastal areas of freshwater runoff were approximately three times more likely to be seropositive for T. gondii compared to otters living in areas of low-flow runoff.3 Therefore, land-based surface runoff appears to be the mechanism by which infective T. gondii oocysts enter the marine environment.
The exact means by which sea otters and other marine mammals acquire T. gondii in the marine environment is unknown. Previous laboratory studies demonstrated that T. gondii oocysts may be concentrated by filter feeding marine bivalves such as mussels, but more recent research has shown that specific feeding preferences of sea otters also may affect toxoplasmosis prevalence. Sea otters with diets composed of > 10% marine snails were 12 times more likely to be infected with T. gondii than sea otters that ate fewer marine snails. In contrast, sea otters with diets consisting mainly of abalone had a much lower risk of infection.4 In another study, the specific physical properties of T. gondii oocysts (i.e., the loss of electrical charge in saline waters) was shown to promote flocculation and sedimentation of T. gondii oocysts in areas where marine and fresh waters meet, such as estuaries and near-coast habitats. These are areas where marine snails and sea otters frequently feed, but also where humans may be more exposed by water-related activities to infective oocysts as well.5
Several human toxoplasmosis outbreaks have been epidemiologically linked to contaminated water sources, including one outbreak in a municipal water reservoir in British Columbia, Canada.6 It is also known that wastewater treatment practices and chlorination are not effective at destroying the oocysts of T. gondii, and they can remain viable in seawater for up to six months. The Palo Alto Medical Foundation Toxoplasma Serology Laboratory in conjunction with the CDC recently published a case control study of 148 adults infected with T. gondii. In this study, eating raw oysters, clams, or mussels was a risk factor for acquisition of toxoplasmosis in the subset of patients asked this question. Other risk factors were eating raw ground beef or rare lamb, working with meat, eating locally produced cured, dried, or smoked meat, drinking unpasteurized goat's milk, and having three or more kittens.1
It is estimated that 32% of households in the United States own cats (an estimated 78 million cats); an additional 73 million cats are feral.7 With these large numbers, the potential land-to-sea transport of infectious T.gondii oocysts is impressive. Cat owners can help by not flushing cat litter down the toilet. Instead, cat litter should be bagged and disposed of in approved landfills where runoff is well controlled. This includes cat litter products that are advertised as "flushable litter." Some cat litter products may even be advertised as "eco-friendly" to be added to compost piles, but this should be avoided as well. In 2006 California Governor Arnold Schwarzenegger signed a bill into law requiring that all cat litter sold in California carry a warning label not to dispose of the litter in toilets or storm drains. However, many people remain unaware or perhaps unconvinced of the importance of this law.
What is in our backyards, be it cat feces or the chemicals used in our homes or lawns, invariably will end up in our oceans. The connection between the health of marine mammals and human health is more evident each day. Scientists in both realms now realize that the environment we share together means we share the same risks and, eventually, the same fates. As Jean-Michel Cousteau, the renowned explorer and passionate advocate of protection of the marine environment, tells us, "Protect the oceans, and we protect ourselves."
More information about marine conservation and sea otter research can be found at www.oceanfutures.org and www.seaotterresearch.org.
References
- Jones JL, et al. Risk factors for Toxoplasma gondii infection in the United States. Clin Infect Dis 2009;49:878-884.
- Dubey JP, Jones JL. Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol 2008;38:1257-1278.
- Miller MA, et al. Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). Int J Parisitol 2002;32:997-1006.
- Johnson CK, et al. Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system. Proc Nat Acad Sci 2009;106:2242-2247.
- Shapiro K, et al. Surface properties of Toxoplasma gondii oocysts and surrogate microspheres. Appl Environ Microbiol 2008;75:1185-1191.
- Bowie WR, et al. Outbreak of toxoplasmosis associated with municipal drinking water. Lancet 1997;350:173-177.
- Conrad PA, et al. Transmission of toxoplasma: Clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int J Parasitol 2005;35:1155-1168.
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