Spore concentration and modified host resistance as cause of anthrax outbreaks: A practitioner’s perspective

Most of what is written about the cause of anthrax outbreaks is by professional academics in the fields of microbiology, epidemiology, and pathology. Little has been written by veterinary practitioners as it is normally not part of their job. Academic contributions could be closer to the actual fact and could be more useful if they recognized a practitioner’s humble experiential intuition.

Hugh-Jones and Blackburn (1) comprehensively reviewed virtually all the theories on the etiology of anthrax outbreaks. They append a summary of 4 points that emphasize the need for more information on the existence or non-existence of spores in soil, the role of tabanids, latent infections, and modified host resistance. They note that the cause-and-effect answers that would scientifically demonstrate the resolutions to these questions would be an enormous undertaking. However, answers exist from work already done.

The Russians have considerable knowledge on anthrax. Before they developed an effective vaccine and management practices, the infection was widespread, especially in the vast Eurasian steppe. The most dramatic outbreaks followed the Soviet’s extended farming push northward during the early 1920s that introduced livestock and, by extension, anthrax to the shores of the Arctic Ocean, as well as to the enormous herds of hitherto uninfected reindeer. The worst was in Yamal district where hundreds of thousands of animals died each summer, giving birth to the oft-used discriptor “Yamal” disease for such exceptionally large outbreaks. Starting about 1930, vaccination and management practices proved highly effective, especially in the North. After years of no anthrax, these programs were scaled down or discontinued until outbreaks again occurred. Over time, in the North, anthrax was deemed to be eradicated, or so seemed the case until 2016 when changing climatic conditions caused an ancient permafrost pit — once used to dispose of carcasses — to thaw out, thus triggering a local outbreak. Fortunately, due to quick action on the part of locals, it was immediately contained.

The foremost Russian researcher, G.V. Kolonin (2,3), benefited from his shared veterinary and geographical backgrounds. He noticed the striking difference between the effectiveness of the vaccination and management programs in the far North and those of the steppe region. Hugh-Jones and Blackburn (1) point this out on a global scale through the use of computers. Kolonin (2,3) argues that the soils in the south are more conducive to the existence of anthrax spores than are the northern more acidic ones. Without the soil-storing spores acting as a source of infection, the disease must be transmitted from host to host. This is because resistance of reindeer allows the disease to exist in a latent state most of the time. Anthrax develops as a peracute infection when the extremely oppressive insect harassment during high summer reduces the populations’ resistance to low levels, and tabanids transmit the bacterium. Hugh-Jones and Blackburn (1) label the Yamal example the modified-host resistance model, and the steppe example they call the spore-concentration model; they conclude that both are unproven. However, Kolonin (2,3) describes the phenomenon as a gigantic field experiment and that the enormous numbers involved cannot be ignored. On my part, I warmed to these Russian findings during 2 trips to Finland in 2011 and 2014 (4) and 2 trips to Russia in 2016 (5). As a retired veterinary practitioner with a lifetime career involvement with the disease, I find their ideas have merit because they make uncomplicated sense.

Hugh-Jones and Blackburn (1) spend a lot of their review on Africa, which is useful up to a point. Virtually anywhere there are concentrations of animals, wild and domestic, the disease is a problem. Vaccination is usually only a temporary solution implying the soil preserves the spore and is the source of infection. The species particularly associated with the disease is wildebeest. In most areas of the world, wildebeest short grasslands and game sanctuaries support grain crops and/or grazing livestock. Wildebeest was the host species for my 3-year field study of the population effects of anthrax in the Selous Game Reserve (6). At the time, I assumed spore concentration was the cause of the outbreaks, but after learning of “Yamal” disease, I recognize now that involvement of modified host resistance also makes sense. Environmental conditions during the anthrax season became extremely oppressive as the hot, rainy season brought with it an overwhelming presence of tsetse flies, leading some biologists to dub the Selous in the rainy season “Devils Island.” As well the effect of overgrazing, drought, and lack of water was often a common problem, there and in other notorious anthrax areas. During my year in Ethiopia as a field veterinarian for domestic animals, I observed that vaccination programs were well-adopted, as they generally were throughout most African livestock areas. In most reports, tsetse flies are usually commented upon, and indeed Hugh-Jones and Blackburn (1) point out the almost universal presence of disease-bearing tabanids. Considering the disease’s association with terrible environmental conditions, in Africa modified host resistance must also be considered a factor.

When I first visited the Selous, I conducted a necropsy on every carcass I came across in the field for a general survey of parasites and diseases of animals in an enormous wilderness area with no history of human disturbance; that is, an area of natural host-parasite relationships (6). Anthrax was suspected by previous biologists and veterinarians, but was not confirmed despite many submissions for culture and histopathology. A Canadian pathologist, Bob Lewis, suggested I take lab mice into the field and inject them with carcass fluids as soon as possible. The mice that died were to be frozen for transport and shipped to the closest diagnostic lab. Eight of nine mice came back positive for anthrax (7), and I stopped doing necropsies on carcasses that may have been anthrax-infected. Of the 8 confirmed and approximately 20 of my suspected field necropsies, none showed the macroscopic features considered to be diagnostic of the disease at that time. Eventually I did notice that the retro-pharyngeal lymph nodes were enlarged in some, but not in all. Mostly they differed little from the normal healthy animals we shot and necropsied routinely for food and other purposes. I did learn that blood smears stained to show capsules and bacilli were solid evidence of the disease.

As an aside, the work in the field did not involve protective clothing, gloves, or even cleaning solutions. Surprisingly, none of the humans developed septicemic anthrax, although in my 3 years of residence 3 out of 3 Canadian volunteer biologists (including myself ) and 1 of 5 African assistants contracted carbuncles on our hands. All 4 cases responded promptly to a 10-mL IM injection of veterinary benzathine and procaine penicillin G, the only option for a remote and isolated location. Himsworth and Argue (8) point out that many people will recover from the cutaneous form without treatment.

Hugh-Jones and Blackburn (1) describe the Great Plains of North America as a natural anthrax area. This enormous historic grazing area has been greatly reduced by grain cultivation and is shrinking daily as new farming methods come on-stream. Outbreaks of the disease still occur (9–11) but usually only sporadically after transport of cattle or bison. Vaccination often eliminates the problem. In a few areas, vaccination needs to be continued but other evidence suggests that the host-to-host or modified-resistance form pervades. Bison seem to be more afflicted on a per-head basis than other livestock species. Bison may be similar to reindeer in that they have adapted to the host-to-host form of the disease. I practiced in Alberta and Canada’s North for over 30 years as a large-animal veterinarian, and I found that very few of the animals which died were professionally examined. Only when the owner suspected he may have had a serious problem would he ask the local practitioner to necropsy and submit samples. Of the animals I examined, very often they looked healthy with no diagnostic lesions and the submissions would come back inconclusive. Our answers were suggestive of common problems other than anthrax, but I often wondered if there were correlations to my study in the Selous and if some were actually anthrax. This suggests to me that many of the thousands of animals which die each year could actually be anthrax-related.

Unfortunately, only when a significant problem arises is it rigorously investigated, so the numbers are absent in this respect. Himsworth and Argue (8) examined the clinical signs and gross pathology of several carcasses submitted to diagnostic labs in Saskatchewan that were eventually diagnosed with anthrax and have drawn up helpful guidelines for fieldwork.

The northernmost extension of Canada’s Great Plains hosts 2 prominent anthrax areas: Wood Buffalo National Park and the nearby McKenzie Bison Sanctuary. Both have classic soils for the maintenance of spores and have undergone several studies (12–14) which point this out. Gates et al (13) go further to suggest that, because the outbreaks occur at a time before the bison are stressed by the rut, spore concentration in the soil and unmodified host resistance must be the cause of the outbreaks. However, they did not adequately consider as a stressor the extremely oppressive tabanid season which runs June 15 to July 15, the exact time of the outbreak in question. The Russians would not have agreed. When I owned cattle and horses and practised large-animal veterinary medicine for 10 years in Northern Alberta and the southern Northwest Territories (both in close range to these 2 anthrax areas), the most limiting factor for livestock production was by far the summer insect season (15,16). Without protection, animals would predictably lose weight, and those strays off by themselves would be especially afflicted. When handling horses at this time of year, my hands were often covered with their blood. The worst time of year for horses and bison was the relatively short tabanid season; for cattle it was the longer blackfly season. Not recognizing the possibility that insects, especially tabanids, could modify bison resistance is a major omission by Gates et al (13).

Hugh-Jones and Blackburn (1) emphasize the need for more extensive study of spore activity in the soil, the role of tabanids, latent infections, and modified-host resistance. My lifetime experience and practitioner’s intuition tell me we already have the answers, but the weak link in this chain of research is that academics have failed to listen to livestock owners, practitioners, and Russian knowledge in regard to modified host resistance. They are in the best position to evaluate the host population’s relationship to its environment and its resistance to this disease. For a large portion of an indigenous population to suddenly come down with only the peracute form of the disease, the environment must have changed its relationship with the host.