One Health, Ethics, and Controlling Zoonoses

Recently, a commentary on the practice of culling animals to reduce the risk of zoonotic diseases (Johansen and Penrith 2009; ) caught my attention. The authors were making note of a study in China by Xianget al reporting on an intervention to control a parasitic disease (cystic hydatiddisease) caused by the dog tapeworm Echinococcus granulosus. The lifecycle of Echinococcus granulosus is fairly complex (interested readers can see a nice diagram at the CDC website) but in short, dogs can serve as the definitive host for the tapeworm, which they get by eating the carcasses of sheep or other infected animals. Infected dogs then pass eggs in their feces which can be ingested by and infect humans or other animals. In humans, the tapeworm can develop and cause expanding cysts in the liver, brain, lung and other tissues which can be associated with serious illness (hydatid disease) including abdominal pain and seizures.

At any rate, the goal of the Chinese researchers was to reduce the rate of hydatid disease in two Chinese counties. In these counties, with a combined human population of about 255,000 ,  the annual rate of hydatid disease was estimated at about 44/100,000, or roughly 112 cases per year, of which as significant percentage required surgery to remove cysts. The researchers’ disease control strategy was to stop the dogs in the area from eliminating the parasite eggs into the environment through their feces. To do this, the research team attempted to treat all the registered dogs in the study area each month with praziquantel, an antiparasitic medication that could eliminate the worm. At the same time,  they captured and “humanely” killed stray and unwanted dogs in the two study counties. According to the report, 10,575 dogs were killed as part of the intervention. (The authors noted that there were more stray dogs in one of the counties with a higher proportion of Muslims, who avoid eating dogs as meat, in the other, largely non-Muslim, county, dogs were a source of food for humans and there were fewer strays). A small fee charged to dog owners paid for the treatment and culling of the dogs.

The study reported that the intervention strategy successfully reduced the prevalence of hydatid disease in sheep to virtually zero, and also reduced the rate of infection in dogs (who usually have few symptoms from the infection).
In their commentary about the study, Johansen and Penrith state that “culling animals has been used in many parts of the world as a highly effective way to control and eliminate various infectious diseases of both veterinary and human health importance” (culling of poultry has been a major tactic in the effort to control outbreaks of avian influenza)  but that such culling programs raise “ dilemmas regarding ethics, validity of the research, and research ethical questions”. In particular, Johansen and Penrith argue, the evidence supporting the use of culling should be carefully considered, as should the social, economic, and cultural impact on local populations. 

The concept of “One Health” , which has received a lot of attention recently (see Kaplan et al 2009) may also provide some new perspective to debates over the culling of animals to control zoonotic disease. While definitions vary, One Health has been described as:  
“The collaborative effort of multiple health science professions, together with their related disciplines and institutions – working locally, nationally, and globally – to attain optimal health for people, domestic animals, wildlife, plants, and our environment.”

Following the One Health line of reasoning, what does it truly mean to “attain optimal health for people, domestic animals, wildlife, plants, and our environment.”?  There appears to be an implicit assumption that this can be a win-win situation all around, and that what is good for the people can also be good for the animals, plants, and the environment.
While this is a very attractive proposition, the methodology of the Xiang study suggests that the reality ‘on the ground’ is not all win-win. Their hydatid disease control strategy (which has now been replicated in other parts of China) appears to have been good for humans, sheep, and registered dogs, and also perhaps good for the environment (less contamination by dog tapeworms), but it was decidedly not good for the stray and unwanted dogs. I wonder, however, how often this has been tested in reality. If one wants to control a disease like cystic hydatid disease, what is the way to do it that maximizes the health of people, animals, and the environment? If there are tradeoffs to be made, how are those judged? The Xiang study provides some hard numbers for the choices made in one case: 10,575 dogs culled to prevent a several hundred human cases of a parasitic disease.

I have previously discussed culling as one of the aspects of the  “us vs. them” attitude that human health professionals may take toward when faced with potential health risks of zoonotic or other animal-associated diseases. (See Rabinowitz et al 2008) . In that paper, we argue that it may be useful to move from the “us vs. them” approach toward a model of “shared risk” between humans and animals facing increased disease threats from the environment. The “shared risk” approach requires an examination of the changing environment and whether it could be driving disease risk in both animals and humans. In the case of Echinococcus-caused hydatid disease, for example, have there been changes in the density of sheep, dogs, and humans that make the disease risk more intense? If so, could environmental measures, such as better fencing or other measures to keep dogs away from sheep carcasses, play a role in disease control? Are there other ways to deal with stray dogs besides culling (such as spay/neuter programs). It is interesting to note, that for rabies, another dog-associated zoonosis, researchers have proposed that in China, immunization may replace culling as an effective control strategy (see Zhang et al ) . In short, are there alternative ways to maximize the health of the humans, animals, and the environment in order to achieve the closest thing to a win-win situation? There may be tradeoffs between short term and long term successes, and what works in the short term (culling dogs) may not necessarily address some long term environmental issues that are driving disease risks.

These cases suggest the need to examine the ethics underlying a One Health approach to zoonotic disease control and other diseases at the human-animal- environment interface. They also indicate that we have to strive to better understand the complex interactions that lead to emerging infectious diseases, and the tradeoffs required to control and prevent such diseases in the future.