Clinical impressions of anthrax from the 2006 outbreak in Saskatchewan

Abstract

Clinical signs and carcass traits observed during the 2006 Saskatchewan anthrax outbreak were largely consistent with those previously published, except for cutaneous anthrax and anthrax mastitis in cows, and subcutaneous edema in bulls and horses. Failure of blood to clot was the most reliable indicator of anthrax in carcasses.

In the summer of 2006, an anthrax outbreak occurred in the east-central area of Saskatchewan. According to Canadian Food Inspection Agency (CFIA) records, over a 3-month period between June 26 and September 21, 804 animals on 153 premises were affected by anthrax, making it the largest anthrax outbreak recorded in Canada. The 804 animals included 493 cattle, 254 bison, 33 sheep, 13 cervids (white-tailed deer and elk), 6horses, 3 pigs, and 2 goats. This outbreak was of interest not only because of its size and the variety of clinical syndromes that were anecdotally reported, but also because news of an outbreak caused practitioners to anticipate cases of anthrax, so they were particularly alert to the varied manifestations of the disease.

The present study reports the clinical signs and carcass traits of 245 cases of anthrax identified in cattle, bison, and horses during the outbreak; its intent is to compare the clinical observations with those previously described in order to update and/or reaffirm those in the literature and thus improve clinical recognition of the disease in future outbreaks. Of the 51 live animals, 43 were cattle, 4 bison, and 4 horses. Of the 194 carcases, 162 were cattle, 27 bison, and 5 horses.

According to the literature, the presentation of anthrax in live animals depends on the host species, the bacterial strain and dose, and the route of infection (1). Ingestion of contaminated soil or animal products is thought to be the most common route of infection in most anthrax outbreaks in animals (2,3). Percutaneous transmission from biting tabanid flies is possible, but of unknown significance (2,3). Inhalational transmission of anthrax is rare under natural conditions (2).

Most ruminants are thought to exhibit a peracute form of the disease following ingestion of anthrax spores, which is characterized by a clinical course lasting 2 h, before death occurs (1,4). The most common presentation of this form is a dead animal without a history of any previously noted clinical signs (1). Occasionally, if an animal with this form is found alive, it may exhibit marked pyrexia and restlessness or anxiety; have pronounced dyspnea and congested, hemorrhagic, or cyanotic mucous membranes; and, in the terminal stages, exhibit muscle tremors or convulsions (1,4).

Less commonly, ruminants may develop the acute form of anthrax, which is characterized by a slightly longer clinical course, with more varied and nonspecific clinical signs (1,2). These animals may show signs that are similar to those of the peracute form; however, rather then being restless, they are often depressed and anorexic, with accompanying ruminal stasis (1,2). In addition, there may be edematous swelling in the oropharynx and areas of the subcutis, and small scattered hemorrhages in the skin and mucous membranes (1,2). Hematuria and digestive disturbances, such as diarrhea and dysentery, are not uncommon (1,2,5). Pregnant animals may abort, and lactating animals may experience decreased milk production and, possibly, bloody or yellowed milk (1,2,5). If the animal is left untreated, death is sure to follow within 2 to 3 d (1,2).

Although unusual, pulmonary anthrax due to inhalation of spores has been reported in cattle (6). Such cases also tend to follow an acute clinical course, with the distinguishing feature being the presence of a marked productive cough (6). It has been suggested that wallowing activities in bison bulls (vigorous rolling, particularly in dusty soils) may allow sufficient aerosolization of spores to support a respiratory route of infection in some cases (7,8).

Percutaneous transmission of anthrax in cattle due to biting flies can result in a more protracted form of the disease, distinguished by edematous swellings in the regions of the shoulders, ventral neck, and thorax, presumably associated with fly bites (5,9).

Horses are most likely to develop an acute form of anthrax and, without treatment, most will die within 2 to 4 d of the clinical onset (1,5). They usually present with 1of 2 common clinical syndromes. Some demonstrate focal or generalized subcutaneous edema of the abdomen, thorax, legs, perineum, and the external genital area, possibly as a result of anthrax transmission by biting flies (1,2). Alternatively, ingestion of anthrax spores can lead to fever, depression, and gastrointestinal lesions, such as oropharyngeal swelling, enteritis, and colic (1,2).

Regardless of species, in cases where the animal is found dead, carcass characteristics include bloody exudates emanating from the body orifices and failure of blood to clot (1,4,10). In addition, there may be an absence of rigor mortis and overly rapid putrefaction of the carcass (1,4,10). In bison, bloody discharge from body orifices is an inconsistent postmortem finding; however, carcasses of this species may have the additional characteristic of sloughed cape hair and white frothy discharge emanating from the nose and mouth (8).

To compare the clinical impressions of the 2006 anthrax outbreak with the picture presented above, 19 veterinarians (15 private practitioners and 4 veterinarians employed by the CFIA) were interviewed in June 2007. All veterinarians had personally examined animals afflicted with anthrax during the 2006 outbreak. Information was collected on cases considered positive for anthrax, and practitioners were instructed to include only those animals that they had personally examined when answering the questions.

Included were animals that had received a positive laboratory diagnosis for anthrax (positive culture results from either Prairie Diagnostic Services, Saskatoon, Saskatchewan, or the CFIA/ OIE Reference Laboratory for Anthrax in Lethbridge, Alberta). Also included were animals that were not tested but had been diagnosed by a veterinary practitioner as anthrax-positive on the basis of their geographic proximity to other anthrax cases, in combination with a clinical evaluation that was suggestive of anthrax. Due to financial and practical considerations in the field, the incentives for doing extensive laboratory testing and keeping strict records for anthrax cases are minimal, so clinical surveys are the most potent tool by which to track changing patterns of clinical presentation.

The results of this survey, summarized in Tables 1 and 2, reveal that, in general, the clinical signs and carcass traits for anthrax observed during the 2006 outbreak were consistent with those previously reported; however, there were several notable differences and unique clinical presentations that warrant further discussion.

Table 1.

Clinical signs observed in live anthrax-positive animals: Number of animals showing each clinical sign

	Species
Clinical sign	Bovine	Bison	Equine
Fever	2 (4.7%)	0	3 (75.0%)
Restlessness/anxiety	5 (11.6%)	0	0
Depression	15 (34.9%)	4 (100%)	3 (75.0%)
Tachycardia	0	0	2 (50.0%)
Dyspnoea	8 (18.6%)	0	0
Coughing	2 (4.7%)	0	0
Muscle tremors	7 (16.3%)	0	0
Convulsions	7 (16.3%)	0	0
Ataxia	2 (4.7%)	0	0
Abnormal mucous membranes	0	0	0
Antemortem hemorrhage	6 (14.0%)	0	0
Subcutaneous edema	13 (30.2%)	0	4 (100%)
Skin lesions	22 (51.2%)	0	0
Digestive disturbances	5 (11.6%)	0	0
Changes in milk	1 (2.3%)	0	0
Total animals	43	4	4

Note: A full clinical examination was not performed on all of the live anthrax-positive animals (including the bison), either for practical reasons or because it was not deemed necessary by the practitioner due to a high suspicion of anthrax.

Table 2.

Carcass traits observed in anthrax-positive animals: Number of animals showing each carcass trait

	Species
Carcass traits	Bovine	Bison	Equine
Bloody fluids exuding from body cavities	140 (86.4%)	16 (59.3%)	1 (20.0%)
Failure of blood to clot	156 (96.3%)	26 (96.3%)	3 (60.0%)
Darkened blood	123 (75.9%)	24 (88.9%)	2 (40.0%)
Absence of rigor mortis	90 (55.6%)	18 (66.7%)	1 (20.0%)
Over-rapid putrification	72 (44.4%)	19 (70.4%)	0
Subcutaneous edema	12 (7.4%)	0	3 (60.0%)
Skin lesions	4 (2.5%)	0	0
Abnormal mucous membranes	14 (8.6%)	0	0
Signs of convulsions (disturbed ground around the carcass)	13 (8.0%)	0	1 (20.0%)
Total	162	27	5

Note: Carcass traits of anthrax requiring close examination to detect (subcutaneous hemorrhages, oropharyngeal edema, and changes in mucous membranes) may have been missed in some cases, since attempts to minimize carcass handling and exposure of the veterinarian to a potential zoonosis often meant that carcasses were examined only at a distance before sampling and/or disposal.

It has been suggested that most of the ruminants suffering from anthrax experience the peracute form of the disease, characterized by sudden death with few or no premonitory signs (1,4). This was true for the 2006 outbreak: of the 236 ruminants described in this study, 189 were found dead without a recognized period of sickness, despite increased surveillance during the outbreak. Also, of the 43 cattle found alive, 6 exhibited clinical signs consistent with this form of the disease including dyspnea, muscle tremors, convulsions, lack of response to treatment, and rapid progression to death. However, those 6 also exhibited marked depression, bordering on nonresponsiveness, contrary to the restlessness or anxiety reported in the literature (1). In addition, profuse antemortem hemorrhage from the nose and mouth was reported in at least 2 cases, a sign of anthrax that does not appear to have been regularly reported.

At least 16 of the 43 cattle observed alive appeared to have been suffering from acute anthrax. These animals showed typical signs (1,2,5); however, dysentery and abortions were not seen. Of interest in this group was the preponderance of live anthrax-positive bulls exhibiting scrotal and preputial edema as a prominent or predominant clinical sign, not commonly reported. In many species, edematous swellings of the scrotum and prepuce have been reported secondary to a number of bacterial, viral, and parasitic infections, including the toxin producing Clostridium difficile, which is related to the anthrax bacterium (11). However, the exact mechanism for the subcutaneous edema specifically affecting the male genital area does not appear to have been clearly elucidated.

Most animals affected by anthrax during the 2006 outbreak had the systemic form, presumably caused by ingestion of spores; however, at least 20 live cattle appeared to be suffering from cutaneous anthrax. Rather than developing edematous lesions (5,9), these cattle appeared to experience a form of the disease that most closely resembles human cutaneous anthrax, where “echars” or necrotic lesions in the skin develop (12). The lesions varied in number, were up to 10 cm in diameter, and were located on one or both sides of the body in the middle to caudal thoracic region. They began as expanding areas of dark, necrotic skin that eventually sloughed off, leaving a bloody and crusted epidermal defect that healed in a few weeks without treatment. These animals were not clinically ill and demonstrated no other clinical signs characteristic of anthrax. The lesions may have been caused by percutaneous transmission from biting flies carrying the infective spores, or through minor skin wounds as a result of the cattle being moved through an anthrax spore-contaminated chute system.

Although cutaneous anthrax in animals is not well understood, in humans, it is accepted that up to 90% of these skin lesions will heal spontaneously (12), which is consistent with what was observed in the affected cattle. However, in humans, cutaneous anthrax has a 5% to 20% chance of mortality due bacteria spreading from the lesion and causing a fatal septicaemia and/or complications, such as anthrax meningoencephalitis (12,13), neither of which was seen in these cattle. All of the animals thought to be suffering from this form of the disease had previously been vaccinated against anthrax; therefore, it is possible that the vaccine afforded some degree of protection against the harmful sequelae of the disease. Similarly to what was experienced with these cattle, difficulties have been encountered in culturing the anthrax bacterium from cutaneous lesions in humans, and histopathologic examination is often needed for etiological confirmation (14).

The case of anthrax mastitis in 1 cow is exceptional; although changes in milk have been noted secondarily in animals systemically affected by anthrax, in this particular cow, the udder appeared to be the source of the infection and, aside from the mastitis, the cow showed few other clinical signs of the disease. This form of anthrax had not been reported prior to this outbreak.

Overall, carcass traits observed in cattle that had died of anthrax were consistent with those described in the literature (1,4,10). The most common findings included, in descending order, failure of blood to clot, exudation of blood from body orifices, and darkened blood color.

In live bison, marked depression and separation from the herd appeared to be the most prominent clinical sign of the disease. This is consistent with previously reported cases in this species, which suggests that bison may show few signs of the disease until just before death (8,9). In fact, at least 1 depressed animal was observed to die within 15 min of clinical recognition without having demonstrated any other clinical signs. Although previous reports of anthrax in live bison have described ataxia and a stiff-legged gait during the terminal stages of the disease, this could not be confirmed in this study, as none of the live bison were observed in motion.

Sloughed cape hair and foamy discharge coming from the body orifices of dead bison, which has been reported in other outbreaks (8), was not observed by any of the practitioners interviewed for this study.

Over half of the observed anthrax-positive horses, both live and dead, exhibited subcutaneous edema (with fever in live animals) as the predominant sign of anthrax. The development of subcutaneous edema in anthrax-infected horses has been reported to be associated with percutaneous transmission of the spores by biting flies (1,2). However, in all of the anthrax-positive horses observed alive, distribution of the edema closely resembled that seen in bulls, that is, in the inguinal, preputial, and ventral thoracic and abdominal areas, which may suggest that, as in cattle, the horses contracted the disease though the ingestion of spores. In this species, spore ingestion is usually reported to cause oropharyngeal swelling and gastrointestinal upset (1,2), neither of which was observed. Two of the horse carcasses, however, exhibited multiple discrete foci of edema, a pattern that seems more consistent with fly bite transmission.

Overall, the results of this study suggest that many of the clinical signs and carcass traits of anthrax reported in the literature are applicable during anthrax outbreaks in the field. However, the clinical impressions of the group of veterinarians interviewed suggest that the disease may also have new or varied presentations that have not yet been well documented. These include cutaneous anthrax and anthrax mastitis in cattle, and subcutaneous edema (particularly in the preputial and inguinal/ scrotal areas) as a predominant clinical sign of anthrax in live bulls and horses. This study also suggests that failure of blood to clot is the most sensitive carcass characteristic of anthrax across all species.