For One Health Approaches to Succeed, Information Needs to Flow

In considering the different aspects of integrated approaches to human, animal and environmental health along a One Health paradigm, so many of the challenges seem to boil down to the challenge of how to get information to flow in ways it has not in the past. Here are some examples:  

Disease Surveillance:

A number of groups, including the National Academy of Sciences have called for the development of systems that integrate human and animal disease surveillance data. This could allow for improved detection of emerging disease threats in the environment, both infectious and toxic. The Yale Human Animal MedicineProject has performed analyses supporting the promise of such data integration.  But at present, disease surveillance is collected separately by human and animal health agencies, and not shared in a systematic fashion. As a result, we are still limited in our understanding of what the occurrence of disease events in animal populations (think white nose syndrome in bats or colony collapse in honeybees) means for human health. The Canary Database is one resource for at least examining this issue. We are also therefore limited in our ability to detect and predict human health problems related to environmental change. It will take political as well as scientific will to reorganize such information sharing, but it needs to happen.

Environmental risk data:

Part of the challenge of integrating human, animal, and environmental health is having adequate data about environmental risks, whether climate change, wildlife populations, or degree of contamination by biological, chemical, and/or physical hazards. While animal disease data can provide “sentinel” information about environmental risk “shared” by animals and humans, there is often a need to better characterize environments: getting this information often involves getting out in the environment and finding out what is going on, and transmitting that information to both human health and public health and animal health professionals.

 Genomic data:

The genomes of humans and animals hold the key to better understanding key differences and similarities between species that could help improve the health of both humans and animals, discovering new approaches to disease detection and treatment- see Zoobiquity.  Yet this information is complex and vast- and to use it better will take development of new technological approaches for comparing and exploring these genetic linkages. In addition, better understanding of the genetic characteristics of the pathogens that cross between humans and animals (such as influenza) can help anticipate and prevent outbreaks of zoonotic diseases affecting both human and animal populations. The Human Animal Medicine Project is working with several efforts to assemble and analyze genomic data about pathogens, including the GAINS database and Zoophy. Recent breakthroughs in DNA sequencing technology have produced vast databases of such genetic information- what is needed is a path through this thicket of data.

The Microbiome:

A related wealth of genetic information is accumulating about the human “microbiome”: the communities of microbes that call our gut, skin, and other surfaces home, and seem to have a large effect on our health and wellness. How do our microbiomes differ from those of our companion animals or other animals that we contact on a regular basis?  Is the sharing of microbes between humans and animals all negative or could there be some positive aspects to it that have evolved over millennia of coexistence between humans and animals? The Human Animal Medicine project is performing some pilot analyses of this in workers with close exposure to livestock.

Occupational Risk:

On a more basic level, when workers have close contact with animals, such as swine workers working in large production facilities, there is a need to supply them (and their employers) with better information about their occupational risk and ways to reduce such risk. Such information, such as the amount of virus or bacteria that is present in the air and surfaces of barns and other facilities may be critical to decisions about how to protect workers and reduce disease transmission. While this may seem to be sensitive information, better awareness of such information could actually benefit both human health (occupational and food safety) as well as the health of the animals. The Human Animal medicine project is piloting such approaches in workplaces.

The promise of One Health is the concept of rapid information flow between human, animal, and environmental health, allowing for early detection and prevention of emerging disease risks. If these pilot efforts and similar initiatives around the globe continue to bear fruit there is a chance that we are moving in the right direction toward a world with improved health across multiple species in a healthy environment.

The Dog That Was A Canary

A 60 year old factory worker was seen at the Yale Occupational and Environmental Medicine Program for an elevated urine mercury level. He worked in a factory making mercury vapor light bulbs. The company doctor had removed him from work because of a high mercury level, but even staying home the level of mercury in his urine continued to rise. The workman’s compensation carrier had questioned whether there could be a problem with his urine mercury testing results.

During the clinical evaluation, the patient recalled that he had brought his work boots home and had been using them for the past several weeks. When he had checked inside his boots, he found beads of mercury under the soles.

As part of his evaluation, the clinic’s industrial hygienist performed a site visit to his home, in conjunction with the State Dept of Public Health. Real time measurement of mercury vapor in the house showed a number of slightly elevated areas. At the site visit, it was also noticed that the patient had a 3 month old German shepherd puppy. Since there was still a question about whether the house was sufficiently contaminated with mercury to cause the patients elevated level, the dog’s veterinarian was contacted (with the owner’s permission) to arrange for mercury testing of the dog. The dog’s urine showed a mercury level that was five times normal!

Both the man and his dog were advised to move out of the apartment, and the apartment was cleaned of mercury. After a month, dog and human returned to the house, and the man’s mercury levels continued to return towards normal.

Mercury is an important toxic exposure in both workplaces and the environment. Elemental mercury (quicksilver) vapor can be inhaled and cause toxic effects to the brain, kidney, and developing fetus. Workers can bring home mercury from work on shoes and clothes and contaminate a home, as in this case. Lead can also be tracked into a house by workers who are exposed at their job.

This case illustrates that pets and other animals can serve as “sentinels” for toxic exposures in the home, just as canaries once warned miners about dangerous gases. In particular, household dogs and cats have provided warning to nearby humans in the household about lead poisoning as well as carbon monoxide poisoning as well as other toxic hazards. Communication between veterinarians and physicians may help detect hazardous exposures affecting both animals and humans. The Yale Human Animal Medicine Project  maintains the “Canary Database” of evidence about animals as sentinels of human environmental health hazards (http://canarydatabase.org).
See for example the Canary summary for animals as sentinels of lead poisoning: 

Lead as Sentinel Exposure

and the following papers in the database: 

Childhood plumbism identified after lead poisoning in household pets.

"Veterinary" diagnosis of lead poisoning in pregnancy

What’s New About “Zoobiquity”?

 I just finished reading my copy of the new book Zoobiquity: What Animals Can Teach us about Health and the Science of Healing, by Barbara Natterson-Horowitz and Kathryn Bowers. It is a ground-breaking book and essential reading for anyone interested in the connections between human and animal medicine. The authors illustrate, through a large number of side by side comparisons, the striking parallels between clinical conditions in animals and humans, and what these similarities can suggest about the root causes of disease (including evolution and environment) and how best to treat them. Readers familiar with “One Health” concepts will find in the book vivid examples of the convergence of human, animal, and environmental health in emerging infectious diseases and animals as sentinels of toxic and infectious hazards in the environment. Yet, it is worth focusing on some of the truly innovative aspects of this book. First, Zoobiquity boldly asserts that by neglecting its comparative medicine roots, clinical medicine itself has gone astray and the medical profession needs to use the perspective of clinical science that spans different species to get back on track. We need to understand mental health problems such as addiction and self-destructive behaviors in the context of evolution and environment, just as naturalists and veterinarians strive to do, and use this perspective to design new treatment and prevention approaches. Similarly, we need to use the same tools of evolutionary and environmental understanding to rethink our approaches to chronic diseases such as obesity and cancer. Second, Zoobiquity builds the strongest case to date for greater development of clinical knowledge of animal health using techniques that are driving evidence based medicine such as randomized trials and large observational cohorts followed over time in order to glean important information useful for both animal and human health. Third, the concepts in Zoobiquity are presented so clearly and documented so extensively that they appear to have struck a chord in both the general population (see Oprah’s 2012 summer reading list) and the medical community that propels the discussion of human animal medicine linkages to a whole new level. Overall, Zoobiquity throws a gauntlet out to the biomedical scientific and clinical community, urging it not to delay further, but instead to set up an effective research and development infrastructure to pilot and test new hypotheses and clinical approaches using this enhanced comparative model It will be fascinating to see who comes forward to accept this challenge.

Human Health Care Providers and Veterinarians Need to Communicate

It is not uncommon for patients to ask me whether an illness in a pet could be related to symptoms they are experiencing. For example, a patient suffering from allergies caused by mold in her house told me about her dog that was being treated by a veterinary allergist. Was it possible that human and dog were dealing with the same problem?

What are physicians or other health care providers supposed to do with such questions and information? Physicians receive no training in veterinary diseases and are not taught how to appropriately respond to these issues. Should a doctor ask more questions about the dog’s illness? Ask to speak to the veterinarian? Is this a useful line of inquiry or mere frivolous waste of time?

Over 60% of U.S. households include at least one pet (Hoff1999), and this proportion is increasing. Often the degree of medical care that the pets are receiving equals or exceeds the medical care happening for humans in the household. There is a basic rule that veterinarians are not allowed to treat human patients (but veterinarians tell me that their clients often ask for medical advice about zoonotic diseases and other conditions). Physicians, for their part, are not supposed to diagnose or treat animals (but tell that to the rural family doctor I met this week who is regularly asked to take care of goats and cows and dogs). At the same time, there are growing similarities between veterinary medicine and human medicine. (Rabinowitz and Conti 2010) Both disciplines use similar blood tests, urine test, and radiological studies to diagnose disease. Both use similar (but not always identical) medications to treat infections, diabetes, and even mental illness. And there can be value in seeing the numerous similarities between medical conditions that manifest in an animal and a human, as physicians such as Barbara Natterson have noted (see her zoobiquity website http://www.zoobiquity.com )

There are a number of specific reasons why physicians and veterinarians need to communicate and collaborate. Contact with pets or other animals can increase the risk of zoonotic (animal to human) disease transmission, especially for children and immunocompromised individuals (Pickering et al 2008, Kaplan et al 2009, NASPHV 2011), and veterinarians can contribute to effective prevention of such transmission. Veterinarians can also work with clients to reduce the risk of animal bites from pets. Beyond the risk of infections and injuries, people may share chronic health problems such as obesity with their companion animals, and be willing to engage in joint preventive behaviors such as exercise programs (Kushner et al 2006). The strength of the human-animal bond may affect psychosocial health, as well as access to medical care (for example; a patient unwilling to leave pets at home to go to the hospital). Drug-seeking patients may request pain medication and other controlled medications from veterinarians on the pretense that it is needed for their pets (LeBourgeois et al 2002).

In addition, illness in an animal may be a “sentinel event” indicating environmental risk for humans (see the Canary database www.canarydatabase.org for more information on this). An example would be allergies due to a common allergen in the environment, or a dog that is diagnosed with a tick-borne disease giving warning about risk to humans who walk  in the same suburban areas as the dog.

Despite all of these apparently obvious reasons for communication and collaboration between veterinarians and human health care providers, real life examples appear to be rare. The practice of medicine is increasingly evidence-based (as it should be), and the lack of published studies documenting the benefit of such encounters between professionals makes it hard to change current practice patterns. At the same time, there are also no studies showing a lack of benefit of such teamwork! In other words, these ideas, however obvious and promising, remain virtually untested.

What are needed are good pilot projects and studies to begin documenting proof of concept of collaboration between human and animal health professionals. These studies could test the acceptability and effectiveness of clinical protocols and materials such as templates for referrals between veterinarians and their human health counterparts. As information begins to flow between the disciplines, the evidence will be able to point future practice patterns in the correct direction. I (and many others) will welcome that day.

References:

Hoff GL, Brawley J, Johnson K. Companion animal issues and the physician. South Med J. 1999; 92:651-9.

Kaplan JE, Benson C, Holmes KH, Brooks JT, Pau A, Masur H. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents. MMWR Recomm Rep. 2009;58(RR-4):1-207.

Kushner RF, Blatner DJ, Jewell DE, Rudloff K. The PPET Study: people and pets exercising together. Obesity 2006;14:1762-70.

LeBourgeois HW 3rd, Foreman TA, Thompson JW Jr. Novel cases: malingering by animal proxy. J Am Acad Psychiatry Law. 2002;30:520-4.

National Association of State Public Health Veterinarians, Inc. (NASPHV); Centers for Disease Control and Prevention (CDC).Compendium of measures to prevent disease associated with animals in public settings, 2011: MMWR Recomm Rep. 2011 May 6;60(RR-04):1-24.

Pickering LK, Marano N, Bocchini JA, Angulo FJ. Exposure to nontraditional pets at home and to animals in public settings: risks to children. Pediatrics. 2008; 122:876-86.

Rabinowitz PM, Conti LA. Human Animal Medicine: Clinical Approaches to Zoonoses, Toxicants and other Shared Health Risks. Elsevier 2010; 432 pp.

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.