The Wolf as a Disease Carrier
By Will N. Graves
“The only way the E. granulosus parasite will be completely eliminated is elimination of wild canids, including the wolf.”
—Will N. Graves
Wolves in Finland
There’s a long history of wolves attacking domestic livestock, semi-wild reindeer, and people in Finland that traces back to before Rome occupied the Scandinavian northland. In response, the Finns would periodically launch campaigns to reduce wolf numbers. In the early 1700s, for example, while some game species were only hunted by noblemen, anyone could kill a wolf on any land, including the private property of another person. Additionally, at least one male from every family had to participate in hunts to control predators.1
In the 1960s, Finland conducted a war on wolves in northern Lapland. Planes were sent into the air with soldiers carrying sub-machine guns to kill the enemy wolf. Wildlife biologist Dr. Karloo Nygren remembers the time well. He says there was “a radio program where the local Game Chief (we have fifteen such in Finland) gave instructions on how to shoot a wolf through the window—what gun and cartridges one should use and how close to the glass one should keep the barrel when the beast is watching through it.”2
The True Concern
The war against wolves in the 1960s and 1970s in northern Finland was not so much about predation but rather a tapeworm carried by wolves that was infecting reindeer and the people who herd them (Echinococcus granulosus) and the horrible illness (Hydatidosis or hydatid disease) created by the tapeworms.
Russian scientists have identified fifty different diseases that wolves may carry—including rabies, hoof and mouth disease, anthrax, and brucellosis—that can affect livestock and/or people. All canids, wild and domestic, can carry many diseases, including those caused by tapeworms. Every dog owner knows that his/her dogs should be periodically wormed, but relatively few realize that some tapeworms carried by canines can infect humans, as well as livestock and wild game, and that these diseases can be deadly.
After the wolf-culling period in the 1960s and 1970s in Lapland, when wolf numbers were severely reduced, shooting and trapping wolves was greatly reduced. Soon, their populations began to rebound. Dr. Nygren wrote in 2010 that, as wolf populations increase, hydatid disease is again on the rise:
It appears to be spreading in my own home area, Karelia, on both sides of the Fenno-Russian border. I am afraid it will not only affect our staple food and essential part of our heritage, moose, but also us directly. Hunters, dog owners, forest workers, and berry and mushroom pickers will indeed be in danger . . . none of it is exaggeration.
The Wolf Disease Problem in the United States
The possibility that wolves transplanted into the United States from Canada by the 1995–96 relocations might carry Echinococcus granulosus was recognized by the US Fish and Wildlife Service. When the 1993 Draft Wolf Environmental Impact Statement to Congress on wolf relocation was made public, it stated that “wolf recovery is unlikely to have any measurable impact on disease or parasite transmission.”3
Veterinarian Jacob Wustner, who developed and coordinated the veterinary part of the 1995–96 wolf relocation program, stated:
We treated every wolf (at least twice) with three paraciticides, including Droncit, which is essentially 100 percent effective against Echinococcus in wolves with a single treatment. It is extremely unlikely that any reintroduced wolf from Canada could have carried Echinococcus tapeworms into the United States.
However, Wustner then conceded that Echinococcus granulosus was already present in the Northern Rockies, and so the wolves could have quickly picked it up as they became established.4
There is considerable disagreement with this statement from experts in North America and around the world. Parasitologist Dr. Delane C. Kritsky, professor emeritus, Idaho State University, writes:
I conducted research for seven years on E. multilocularis in North Dakota during the 1970s, and it is a very dangerous parasite to human beings. However, the species of Echinococcus occurring in wolves and ungulates in Idaho is Echinococcus granulosus, a close relative of E. multilocularis.
E. granulosus is, in my opinion, more dangerous than the strain of E. multilocularis that occurs in the upper Midwest (North Dakota, eastern Montana, South Dakota, and points southeast). The strain of E. multilocularis in the north-central states appears to be relatively non-infective to human beings. However, E. granulosus is more dangerous because it is highly infective to man and, as a parasite of sheep and domestic dogs, it is much more easily brought into homes in Idaho, Montana, and Wyoming where human beings can be exposed.
Utah had a focus of E. granulosus during the 1970s and 1980s, during which time people were dying or undergoing dangerous surgery for the parasite cyst. The Utah focus occurred primarily in rural areas where sheep were raised. My friend and colleague, Dr. Ferron Anderson at Brigham Young University, was conducting research on E. granulosus in Utah. He developed an educational program that primarily endorsed burying sheep carcasses and deworming dogs, which eventually eliminated the parasite in central Utah.
The parasite in Idaho will not be dealt with as easily—and I doubt that it can ever be eliminated as long as wolves are present—because wolves and ungulates (deer and elk) will maintain a sylvatic (wild) cycle, which did not occur in Utah during the 1970s and 1980s. Thus, elimination of the parasite from sheep and dogs, as occurred in Utah, will not be successful as it was in Utah because the wild cycle will continuously provide eggs of the parasite for infection of man and his domestic animals in the future. The only way that the parasite will be eliminated from our area is elimination of the wolf. I have examined coyotes, which can carry both species of Echinococcus, and foxes from southeastern Idaho since 1974 and never found either Echinococcus multilocularis or E. granulosus. Ferron Anderson never found the latter species in Idaho either when he examined canines in Idaho during the 1970s and 1980s; that is, the E. granulosus was never in Idaho until the introduction of the wolf.
Finally, I asked Fish and Wildlife, during one of their public meetings concerning introduction of the wolf (prior to wolf introduction), and was “brushed off” by their “promise” that the wolves introduced to Idaho would be “dewormed,” which action everyone (and especially they) should have known is never 100 percent effective.5
Hydatid Disease
Hydatid disease or hydatidosis is caused by the Echinococcus granulosus tapeworm. According to the US Army, there are six species of Echinococcus that are currently recognized, and all are capable of infecting man. However, E. granulosus is the most likely of the six species to cause serious or lethal illness.6 Echinococcus granulosus is a three-millimeter tapeworm that requires two hosts to complete its life cycle: the final host, which harbors the adult parasite, and the intermediate host, which harbors the larval stage. The adult parasite occurs in the small intestine of carnivores, canines (wolves, coyotes, dogs, and foxes), felines (lion, puma, and jaguarondi cat), raccoons, and their domestic counterparts (dogs and cats). Ungulates—deer, elk, moose, sheep, goats, caribou, reindeer, and antelope in the wild, and domestic sheep, cattle, buffalo, and goats—are the main intermediate host-group. Humans also can be an intermediate host.
According to the Center for Disease Control, the larval stage of Echinococcus granulosus is transmitted as dogs and other canines eat the organs of animals that contain hydatid cysts. Canines pass the parasite to sheep, cattle, goats, and pigs from eggs released in canine feces. Echinococcus eggs can stay viable for up to a year.7
Humans typically are exposed to eggs through handling carcasses and skins, touching infected animals, and contact with feces of infected animals. Those photos you may have seen of people hugging or kissing wolf-dogs or tame wolves potentially spell trouble, unless the animals have been wormed, as wolves are the most common wild carrier of Echinococcus granulosus. All around the world, the people most likely to contract hydatid disease are those who have close contact with dogs that have had contact with either livestock that have the intermediate larval stage or wild, infected canines. This is why the incidence of infection in many areas is highest among women who clean houses, and children who play with dogs. Anyone who tends to sheep and other livestock, and hunters or ranchers who butcher animals also are at risk from contact with the hair of the animals. Thoroughly sanitizing your hands after contact with dogs that may have rolled in wolf scat or are infected themselves is imperative if you live in areas with wolves. When eggs are ingested through contaminated food or water, they hatch in the small intestine, releasing a small larva (known as an oncosphere) that then penetrates the gut wall and enters the circulatory system. The oncosphere is then carried via the circulatory system first to the liver. Typically, 60 to 75 percent localize there as cysts. Echinoccocus granulosus is the most common cause of liver cysts in the world.8
If the larvae pass through the liver, they are carried into the right auricle of the heart and then to the lungs, where they develop into the larval cyst stage called a hydatid cyst. Cysts may become so large and sometimes numerous that organ failures occur. In wild elk, deer, sheep, goats, caribou, reindeer, and moose, nearly all larvae are found in the lungs. Predators that catch and eat infected animals contract the disease from eating the cysts.
While the lungs and liver are the most common places to find hydatid cysts in ungulates, in human beings, it is not uncommon to find them in other organs of the body, including the brain and reproductive organs. Human beings are not the natural host for E. granulosus; therefore, the oncosphere (the larva of the tapeworm), in a sense, becomes lost when entering the blood stream of a human being and can lodge in almost any organ in its body.
After the larvae are established in an organ, growth begins quickly, resulting in a solid mass in which a central cavity soon appears—the beginnings of the hydatid cyst. A membrane soon lines the entire cavity. This membrane is in direct contact with a thin connective tissue capsule separating it from normal host tissue. The hydatid cyst swells and fills with a milky fluid. The larvae grow steadily and are produced in great numbers. Secondary germinal vesicles may develop inside the first cyst, increasing the infected area and the overall size of the cyst. Cysts in the liver may not be detected until discovered accidentally, depending on their size. In the lungs, difficulty breathing and inflammation are common. If a cyst breaks open, then more and more cysts are formed, and they occupy more space and draw vital fluids from the body, resulting in a wide variety of symptoms as they spread through—out the organs and body cavity.
Hydatid disease in the human kidney, spleen, or brain is generally serious. Seizures and paralysis may occur. Osteoporosis of the skull bones is possible. If larvae reach bone marrow, the bones are weakened, resulting in fractures. Spontaneous or traumatic (including surgical) rupture of the cysts may cause severe anaphylactic shock, which can be fatal. Treatment options include medication and surgery. Surgical removal of cysts must be done carefully, without cutting the cyst open. If a cyst is cut, the liquids can spread the disease throughout the entire body.
Detection of hydatidosis is not easy. While the parasites quickly become established in the body, actual symptoms may not appear for some time, as long as ten to twenty years. Often the cysts are not recognized until other illness or body trauma occurs. New ultrasound and serology tests aid detection, but these are not always able to detect hydatid disease. Often infections are ultimately found in autopsies of people who died of other causes.
Prevalence
There is no question that hydatid disease is serious and can be deadly. It is also well established that, among wildlife, wolves are a major carrier. They may ingest larvae by feeding on infected wild or domesticated ungulates, rolling in feces, and licking each other or themselves. The real question is just how common is hydatid disease among people?
An international survey of hydatid disease published in 1977 in the Bulletin of the World Health Organization (WHO) entitled “Hydatidosis: A Global Problem of Increasing Importance” finds that hydatid disease is global and increasing not only where it is endemic but also in countries where it was not previously found.9 The authors—professors of bacteriology and parasitology from Lebanon, Australia, and England—report that, during the nineteenth century, Iceland had the highest prevalence of human hydatidosis in the world. In 1900, it was 25 percent. They attribute this to the prevalence of sheep and dogs, and they note that an aggressive public health effort to control the disease resulted in a significant decline in human cases during the twentieth century. Other areas with high levels of hydatidosis were northern Scandinavia; throughout the Middle East (Israel once reported an average of one hundred deaths a year from human hydatidosis); the Indian subcontinent, where hydatid disease was the most important helminth (parasitic) health problem in Afghanistan,10 and where 22 percent of the adult humans in one village in India tested positive for hydatid disease; the northern part of Russia; North Africa; Alaska and Canada, where the disease is frequently found in Native Americans and Inuits; southern South America, especially Argentina, Chile, Peru, and Uruguay; and Australia, where the disease is most prevalent in the south and west.
The authors conclude: “Prevention is better than cure . . . Unless urgent action is taken to redress this situation, the natural pattern of the disease is likely to change for the worse in the next few years.” Some may argue that, as the WHO article was published in 1977, it does not reflect contemporary times. In response, following are some brief quotes from other articles:
China
According to Weiping Wu of China’s Institute of Parasitic Diseases, quoted in Scientific American in 2005, at least six hundred thousand Chinese are currently infected by the deadly disease, and an additional sixty million are at risk. “It is an epidemic,” he says.”11
East Africa
In 1988, 18,565 nomadic pastoralists, from twelve different groups—living in the vast, semi-desert regions of Kenya, Sudan, Ethiopia, and Tanzania—were screened for hydatid cysts using a portable ultrasound scanner. High prevalence of hydatidosis were recorded among the Die northwestern (5.6 percent) and northeastern (2.1 percent); the Turkana of northwest Kenya; the Toposa (3.2 percent) of southern Sudan; the Nyangatom (2.2 percent), Hamar (0.5 percent), and Boran (1.8 percent) of southwest Ethiopia and northern Kenya; and the Maasai (1.0 percent) of Tanzania.12
A study of 1,149 people in the village of LaPaloma in central Uruguay in 1998 found 5.6 percent had hydatidosis. Almost 20 percent of the dogs in the village were infected.13
Wales
Echinococcus granulosus in sheep and dogs has been known to be endemic for many decades. An analysis of national hospital records for 1974 to 1983 found that the incidence of human cystic echinococcosis was 0.2 cases per million in England, two cases per million in Wales, and the highest rates (5.6 cases per million) occurring in southern Powys County.14
Australia
Scientists believe that hydatid disease came to Australia with sheep and dogs, and today it is most prevalent in sheepherding areas. It was most common in the late 1800s, but between 1987 and 1992, 321 people were diagnosed with hydatid disease in New South Wales and the Australian Capital Territory.15
Nepal
Hydatid disease is of considerable economic and public health significance in Nepal. One study found that 25 percent of the residents of one region showed symptoms of hydatidosis. Testing of blood samples of patients admitted to different hospitals of Kathmandu Valley showed that the disease had slightly higher prevalence among the males (53 percent) and considerably higher prevalence among the thirty-five-or-older age group (76 percent).16
Finland
In northeastern Finland, 25 percent of the wolves today are carrying hydatid disease. The incidence of the disease is increasing, although it is not yet commonly found among dogs.17
Kazakhstan
Kazakhstan has the most wolves per capita of any country in the world. In 2002, researchers reported that human cystic Echinococcus rates increased four-fold within ten years after post-Soviet independence due to dismantling collectives and changes in organized livestock and farming practices.18
Russia
Over five hundred cases of hydatid disease are reported in Russia every year, and the number is increasing. Hydatid disease is on the rise in the Bashkiria region of Russia where fifty-three cases were identified in 2008, which is 1.7 times the number of cases reported the year before.19
Hydatid Disease in Northern Rockies
The relocated wolves came from Canada, where hydatid disease is well known. For example, between 1991 and 2001 in a clinic in Edmonton, Alberta, Canada, forty-two cases of hydatid disease were identified in people ranging in age from five to eighty-seven years—77 percent were female, 41 percent were native (women and children tend to most often contract the disease), 40 percent of the patients had cysts in their lungs, and 55 percent had cysts in their liver. The researchers report that the most common intermediate hosts are barren ground caribou and moose. Studies have shown that 50 percent of the moose in Ontario and British Columbia have hydatid disease.20 Between 2006 and 2008, a team of federal and state veterinarians and biologists—Foreyt, Atkinson, and McCauley—evaluated the small intestines of 123 gray wolves collected in Idaho and Montana, looking for Echinococcus granulosus tapeworms. Reporting their findings in the Journal of Wildlife Diseases in 2009, they stated, “The tapeworm was detected in 39 of 68 wolves (62 percent) in Idaho, and 38 of 60 wolves (63 percent) in Montana. The detection of thousands of tapeworms per wolf was a common finding.”
Intermediate-form hydatid cysts were found in Idaho elk, mule deer, and mountain goats and in Montana elk. The researchers concluded, “To our knowledge, this is the first report of adult E. granulosus in Idaho or Montana . . . Based on our results, the parasite is now well established in wolves in these states and is documented in elk, mule deer, and a mountain goat as intermediate hosts.”21
The extent of human infection in the United States may not be known for years; however, in 2011 a woman in Idaho, who lives in an area where wolves are common, was operated on to remove a large hydatid cyst on her liver.22
What Can Be Done?
Dr. Valerius Geist, who had a relative die of hydatid disease, advises hunters and those with domestic dogs where wolves are present to take the following steps to protect themselves and their pets:
1. To prevent infection of dogs, do not consume or allow your dog to consume uncooked meat or organs of wild or domestic ungulates. If your dog does have access to carcasses, talk to your veterinarian about an appropriate deworming treatment. Deworming your dog and preventing access to carcasses of dead sheep, which should be buried immediately, are important preventive steps.
2. Hunters should not touch or disturb wolf, coyote, or fox scat. Wear gloves when field dressing a canid carcass, and wash any body part that may have been exposed to feces or contaminated fur.
Neospora Caninum
Wolves also may carry a prozoan parasitic disease, Neospora caninum, which so far has not been shown to affect people, but it does cause cattle, sheep, and goats to abort, resulting in considerable economic loss to ranchers and farmers. N. caninum was not identified until 1988, but has since been found worldwide.23 It is a major cause of abortions in ruminants. Adult infected cattle appear healthy, but they will abort at least 20 percent of the time during their lifetime,24 causing millions of dollars in damages every year.25
Like Echinococcus, N. caninum has a life cycle with two hosts—canids as adult hosts and ruminants as the intermediate host. Neospora caninum may be transmitted by dogs, wolves, coyotes, and foxes. Wild, free-ranging wolves make it very difficult to control the disease in areas where there are cattle, sheep, and goats. Ruminants contract the infectious eggs when they feed on grass where there are wolf, fox, and coyote feces.26
When introduced into a herd, up to 90 percent of the unborn calves can be infected. When the brain and nervous system of cows, as well as sheep and goats, are infected, it results in abortions. When canines eat the aborted fetuses and placenta, the disease is spread, as their feces contain oocysts (hardy, thick-walled spores able to survive for lengthy periods outside a host). When ruminants feed where the canines have defecated, they ingest the oocysts, which then infect the dogs, wolves, foxes, and coyotes; the life cycle then begins again. Neospora caninum is now recognized as being worldwide and one of the most damaging of all parasites transmitted to cattle.27 Neospora caninum does not appear to be infectious to people, but in dogs, it has been found that infection can lead to neurological damage.28
In 2011, a team of researchers from the USDA Animal Parasitic Research Laboratory found Neospora oocysts in three of seventy-three necropsied wolves in Minnesota.29 One study in 2004 found 39 percent of 164 wolves from Minnesota were infected with Neospora caninum.30 A study of wolves in Yellowstone National Park published in 2009 found that 50 percent of the wolves tested positive for Neospora caninum, with the oldest wolves most likely to be infected.31
Researchers in Wisconsin also report wolves testing positive for Neospora caninum. As both Minnesota and Wisconsin have a significant dairy industry and wolf populations are increasing in both states, one would expect that Neospora caninum would also be increasing.32 In a 2011 study reported in the Journal of Veterinary Parasitology, Neospora-like oocysts were found in the feces of three of seventy-three wolves in Minnesota examined by necropsy.33
N. caninum has been shown to be a large economic loss to the dairy and beef industry with infected animals being three to thirteen times more likely to abort than non-infected cattle. The researchers also note that the presence of wolves near cattle and other livestock causes the livestock to run about in fear, which adds further stress that also increases abortions.34
Considering there are wild and domestic intermediate hosts in areas where wolves are now found, eradication is very difficult. However, a vaccine has recently been developed that yields partial protection to ruminants.35
Rabies
Rabies is a viral disease normally spread by the saliva of infected mammals that bite others. After being bitten by a rabid animal, the disease attacks the central nervous system, resulting in swelling, which progresses to the brain. Symptoms may appear as early as seven days after a bite to as long as several years. The average incubation time is three to seven weeks. Early-stage symptoms of rabies include malaise and fever, progressing to acute pain, violent movements, uncontrolled excitement, depression, hydrophobia, hallucinations, and delirium. As rabies progresses, violent mood swings may occur before the victim lapses into a coma. If not treated with a vaccine before symptoms begin, rabies is usually fatal. Death typically occurs two to ten days after symptoms appear. Modern vaccines seldom have any side effects beyond those from common influenza shots.
Rabies vaccines for dogs have severely curtailed bites by dogs as a cause of rabies in the United States. In underdeveloped countries abroad, however, dogs are a major vector for rabies. In North America, rabies is most often spread by wild animals, especially raccoons, bats, skunks, foxes, coyotes, and, where they are found, wolves. When animals become rabid, they seem to lose all fear. Thus, a rabid animal becomes easy prey for a predator, and conversely, rabid animals are not afraid of anything. Rabies is present in almost all countries of the world, and especially in Asia, attacks on humans by rabid wolves are not uncommon. There are an estimated fifty-five thousand human deaths from rabies worldwide every year—about thirty-one thousand in Asia, and twenty-four thousand in Africa.36 There were forty-five cases of rabies in the United States between 1995 and 2010; of these, nine are thought to have been acquired abroad. Bats are the most common carriers of rabies in North America.37
Wild wolves can catch rabies. In 2007 in the Alaskan Inuit village of Marshall in western Alaska, a pack of wolves attacked sled dogs, killing three adults and three puppies. A wolf killed by villagers as they drove off the wolves was found to be rabid by the Alaska Department of Fish and Game.38
Wolves are wild ancestors of dogs, but unlike pet dogs, wild wolves do not receive treatment from veterinarians. As a result, the fifty-some diseases they may carry double their negative impact on human settlements. This reality amplifies the need to keep a safe distance between man and Canis lupus.
Endnotes:
1. http://www.ekoi.lt/info/azl/2003/AZL percent2013_15-20.pdf
2. http://www.savewesternwildlife.org/killer-wolves.html
3. http://huntingnewsdaily.com/2011/07/08/idaho-fg-perpetuates-ignorance-with-misinformation/
4. http://missoulian.com/mobile/article_cfd5615e-77ce-11df-bcde-001cc4c03286.html
5. Personal correspondence with Dr. Delane C. Kritsky, Professor Emeritus, Idaho State University, 2011.
6. http://tmcr.usuhs.mil/tmcr/chapter3/intro.htm
7. http://www.cdc.gov/parasites/echinococcosis/epi.html; for detailed life-cycle information, see: www.dpd.cdc.gov/DPDx/html/Echinococcosis.htm
8. http://www.ispub.com/journal/the-internet-journal-of-pulmonary-medicine/volume-10-number-1/unusual-presentation-of-hydatid-disease.html
9. Matossian, R.M., M.D. Rickard, and J.D. Smythe, “Hydatidosis: A Global Problem of Increasing Importance,” Bulletin of the World Health Organization, 1977, 55 (4. 499–507.
10. Pertaining to intestinal worms, such as the tapeworm and the roundworm.
11. Scientific American, July 2005 issue, page 22; http://www.khamaid.org/about_kham/news/hydatidosis.htm
12. http://www.tropicalmedandhygienejrnl.net/article/0035–9203%2889%2990664–0/abstract
13. http://www.ncbi.nlm.nih.gov/pubmed/9790441
14. http://findarticles.com/p/articles/mi_m0GVK/is_4_11/ai_n13609429/
15. http://www.science.org.au/nova/056/056print.htm
16. http://homepage.usask.ca/∼shb292/hydatid.pdf
17. http://www.sciencedirect.com/science/article/pii/S0304401702003813
18. Togerson, P.R., B.S. Shaikenov, K.K. Baitursinov, and A.M. Abdybekova, “The Emergent Epidemic of Echinococcus in Kazakhastan,” Translated, Society of Tropical Medical Hygiene, 2002; 96: 124–8.
19. http://www.wormsandgermsblog.com/2009/01/articles/animals/dogs/echinococcus-on-the-rise-in-bashkiria-russia/
20. http://www.biomedcentral.com/1471–2334/5/34/prepub
21. Foreyt, William J., Mark L. Drew, Mark Atkinson, and Deborah McCauley, “Echinococcus Granulosus in Gray Wolves and Ungulates in Idaho and Montana, USA,” Journal of Wildlife Diseases, 2009: 1208–1212.
22. http://www.sciencedirect.com/science/article/pii/S0304401711003566
23. Dubey, J.P., “Neosporosis—The First Decade of Research,” International Journal for Parasitology. 29 (10), 1485–8.
24. http://www.wvdl.wisc.edu/PDFpercent5CWVDL.Info.Recognizing_and_Preventing_Neosporosis_Infections.pdf
25. http://cmr.asm.org/content/20/2/323.abstract
26. http://www.ars.usda.gov/Main/docs.htm?docid=11007
27. http://www.merck-animal-health-usa.com/binaries/NeoGuard_Fact_Sheet_tcm130-126564.pdf
28. Barber, J.S., C.E. Payne-Johnson, and A.J. Trees, “Distribution of Neospora Caninum Within the Central Nervous System and Other Tissues of Six Dogs with Clinical Neosporosis,” Journal of Small Animal Practice 37 (12): 568–74.
29. “I am a Woman with a Story to Tell,” The Outdoorsman, March–May, 2011: 7–9.
30. http://dnr.wi.gov/org/land/er/publications/pdfs/wolf_impact.pdf
31. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2738425/
32. http://www.wvdl.wisc.edu/PDF%5CWVDL.Info.Recognizing_and_Preventing_Neosporosis_Infections.pdf
33. J.P. Dubey, M.C. Jenkins, C. Rajendran, K. Miska, L.R. Ferreira, J. Martins, O.C.H. Kwok, and S. Choudhary, “Gray Wolf (Canis lupus) Is A Natural Definitive Host for Neospora Caninum,” Veterinary Parasitology, 2011.
34. http://dnr.wi.gov/org/land/er/publications/pdfs/wolf_impact.pdf
35. http://www.merck-animal-health-usa.com/binaries/NeoGuard_Fact_Sheet_tcm130-126564.pdf
36. “Rabies,” World Health Organization, September 2011. Retrieved 31 December 2011.
37. “Rabies Surveillance Data in the United States,” Centers for Disease Control and Prevention; http://www.cdc.gov/rabies/
38. http://usatoday30.usatoday.com/news/nation/2007-11-03-798767073_x.htm
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