Anthrax and the Taiga

Woodbury’s recent review of anthrax emphasized that there is always more than one factor contributing to disease, especially when in outbreak form (1). But the current model for anthrax is based on only one cause that was derived from experiments that demonstrated a dose-dependent relationship between the severity of the disease and the oral dose of spores (2,3). Peracute disease and sudden death, the form normally associated with the disease in the field, requires a large oral dose of spores; at lower doses the animal may recover. Infection through the bites of tabanids caused only a mild, subclinical cutaneous infection (4).

Bacillus anthracis exists outside its animal host primarily in its spore state, and food and water contamination have been demonstrated to be sources of infection. Most theories on what causes anthrax outbreaks, especially on a regular basis in nature, have been based on the role the external environment plays in providing an oral, point source form of an enormous quantity of spores.

Based on their studies in Wood Buffalo National Park and the McKenzie Bison Sanctuary, Dragon and Rennie (5) concluded that low-lying areas would have spores drained into them and concentrated. In Kruger National Park, South Africa, vegetation near carcasses was found to be highly contaminated with spores from blowfly activity. In Etosha, Namibia, as waterholes dried up the dose of spores would increase and, the incubator theory speculated that certain seasons and conditions could incubate the spores in the soil, vegetating exponentially and then re-sporulating (6).

There are several problems with the dose-dependent model. The dosages required for a peracute infection can rarely be demonstrated in the field; in fact it is often not possible to find any spores even where they should logically be found (7–10). Germination outside of a suitable animal host, the basis of the incubator theory, is used to explain why spores do not just accumulate endlessly, or are even eliminated in an environment (11,12). Most pointedly, Wyatt (13), discussing the use of anthrax bombs as biological weapons, points out that the doses necessary to cause peracute infections would be adequate only at the point source. As you move further away the dose will be lower and actually, there becomes a point where the infection is so mild it will have a protective, vaccine-like effect on a population. As well, contaminated tabanids, almost always present, could cause subclinical infections that also would have a protective effect.

During inspection of the meat of healthy animals from anthrax areas, anthrax could routinely be cultured from retropharyngeal lymph nodes (14). A significant prevalence of anthrax antibodies in otherwise healthy animals was found in another study (15). The protocol for the Pasteur anthrax vaccine involved 3 levels of vaccine virulence for vaccination programs. Animals from anthrax areas, where it was assumed they already had some level of resistance, could be given the virulent strain; animals not in anthrax areas were to be given the mild strain, followed by the moderate strain, and finally the virulent strain (16). What this suggests is what has already been alluded to: before an outbreak, animals in anthrax areas have a high probability of being exposed to doses of the organism at a level that would not cause peracute infection. Why are they the most likely, not the least likely, to get the peracute infections during an outbreak?

Gainer (9) became fascinated with the disease, studying its effects on the structure of a wildebeest population in Tanzania during the 1970’s, witnessing regular outbreaks in wood bison in the 1980’s while in private practice in northern Canada (8), and then witnessing the disease sporadically in southern Alberta for 20 years during private practice there. In Tanzania and northern Canada, tabanids and other insects were notable, as often mentioned during anthrax outbreaks.

Kolonin (17) describes anthrax in Russia. As in North America, it is just about everywhere, sporadically and enzootically. When reindeer were moved into the Taiga during the summer before vaccination was implemented in 1928 (18) the disease was such a problem that it was called Siberian or “Yamal” disease. In some years, over 100 000 animals would die of it. Kolonin (17) also mentioned that Finland had the same problem. To understand the Russian literature better, in November 2011 Gainer travelled to Finland, took the train north to the reindeer herding area, met Oksanen (a local veterinarian), became friends and collaborated on this note (19,20).

Kolonin (17) does not think the source of infection is in the north; he thinks the animals take it with them internally. By the time they reach the northern Taiga, the insect harassment is unbelievable and “Yamal” disease occurs in unvaccinated animals. In otherwise normal animals carrying an inapparent infection from the south, insects are considered to be the major contributors to the poor state of the reindeer resistance that then allows the precipitation of the peracute and septicemic forms of anthrax. Tabanids then transmit the disease to other animals. Nikolaevskii (18) also points out that the young of the year are rarely affected as much as the older animals, and if they are infected it is only at the end of a prolonged season.

During the winter the herders bring their reindeer into settled areas where the animals often mingle or jointly use the cultivated areas with domestic animals. They can return with the infection in a subclinical unrecognizable form or they may acquire it from overwinter contact with these other animals or their soil.

In summary, the Russian explanation as to why the dose-dependent model does not apply to these animals is that the animals used in the experiments to demonstrate dose dependency would have been well cared for, strong and healthy, and their resistance to disease would have been high; the opposite of these animals in anthrax outbreaks on the Taiga. Invariably where outbreaks occur around the world the animals are usually subject to horrific environmental conditions including insect harassment, drought, starvation, and heat, and their resistance to disease would be low. The Russians can then recognize that insects are an important mode of transmission and that the vegetative stage is an important source of infection, as well as spores, the soil and the external environment. This eliminates the need for a point source of enormous numbers of spores that need to be ingested.

The first thing a stockman or woman realizes about raising livestock during western Canadian summers is the effect of insect harassment on their herds. Even in the south it is considerable, but the further north one progresses, the more serious it becomes. Mosquitoes, blackflies, gnats, and tabanids are the most significant. In the Fort Vermilion area, Alberta’s northernmost farming area, livestock invariably lost weight during the summers. Blackflies were actually the most deadly, but the most intense harassment came approximately from June 15 to July 15 when the tabanids were at their peak.

At Fort Smith, Northwest Territories, partially surrounded by nearby Wood Buffalo National Park, tabanid season severely stressed horses so much that it was considered absolutely essential to provide horses with shelter. A horse without shelter lost weight dramatically even with unlimited food. The rest of the year horses survive quite easily in this area, even on local slough hay and otherwise poor quality feed if the quantity is adequate. Horses in the area reacted to tabanids more than did the cattle, which reacted more to blackflies and the quality of the feed (21,22).

Bison in the nearby national park seemed more like horses, in that they are extremely uncomfortable during tabanid season. Coincidentally, towards the end of the tabanid season and the beginning of the rut, probably as much stress as can be put on an animal, mostly male bison start dying of anthrax in and around the national park, on what is essentially an annual basis. Gail Steed (personal communication, 2012), living on a farm on the edge of the park all her life says she can usually predict a good anthrax season from the tabanid activity and the state of her horses. The only place Gainer has seen worse insect harassment than Fort Smith is the McKenzie Bison Sanctuary, Northwest Territories and specifically Mills Lake. Anthrax also occurs there in bison on a regular basis. Oksanen believes river sides in Finnish Lapland might compete with these areas for mosquitos, but there is little livestock and no anthrax.

The regular outbreaks of anthrax in bison in Northern Alberta, Wood Buffalo National Park, the Slave River Lowlands and the McKenzie Bison Sanctuary most resemble the Russian reindeer situation as they are both in the Taiga with severe insect harassment. The Russian model would lead us to believe that anthrax in these areas could exist either in the soil or in low-grade inconsequential infections within an animal or 2 in a herd. When insect harassment or rut or other stresses lowered these animals’ resistance enough, the peracute septicemic form would occur allowing tabanids and other insects to transmit the bacteria to other animals also with lowered resistance.

The occurrence of anthrax 25 km northwest of Fort Vermilion in 1996, and 35 km south near La Crete in 1975 were beside wetlands and at a time when tabanid activity would be most significant (23). There is similar occurrence in bison and cattle near Prince Albert, on the edge of the boreal forest where tabanids would be a factor (24), and in several other areas of Alberta (25). Pugh and Davies (26), dealing with a massive outbreak of the disease during a prolonged 10-year drought in Zimbabwe, were convinced that tabanids were the primary source of transmission.

The Russian model also may explain why the disease occurs sporadically in other areas that have no history of the disease, and doesn’t recur in the future. Even if bison and cattle that are transported are symptomless, some may have a dormant infection. Anthrax, in a more benign form, may actually be more prevalent in the livestock industry than realized.