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Keywords:

  • Alpaca;
  • Antivenin;
  • Llama;
  • Snake

Abstract

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Acknowledgment
  7. References

Background

Morbidity and case fatality from rattlesnake envenomation is regionally specific because of variability in relative toxicity of the species of snake encountered. A previous report of rattlesnake envenomation in New World camelids (NWC) from the western coastal United States documented high case fatality rates and guarded prognosis for survival.

Hypothesis/Objectives

To describe clinical findings, treatments, and outcome of NWC with prairie rattlesnake (Crotalus viridis viridis) envenomation in the Rocky Mountain region of the United States.

Animals

Twenty-seven NWC admitted to the Colorado State University Veterinary Teaching Hospital for evaluation of acute rattlesnake envenomation between 1992 and 2012.

Methods

Medical records of NWC evaluated for rattlesnake envenomation as coded by the attending clinician and identified by a database search were reviewed retrospectively. Month of admission, signalment, area of bite, clinical and clinicopathologic data, treatments, and outcome were recorded.

Results

Twenty-five llamas and 2 alpacas were admitted for envenomation. Llamas were overrepresented compared to hospital caseload. The face was the most common site of envenomation, observed in 96% of recorded cases. Presenting clinical signs included fever, tachypnea, tachycardia, and respiratory distress. Nine animals required a tracheotomy. Median hospitalization time was 3 days and overall survival rate was 69%.

Conclusions and Clinical Importance

Case fatality rate for prairie rattlesnake envenomation in NWC was lower than that reported in the Western coastal region of the United States and similar to that reported for prairie rattlesnake envenomation in horses.

Abbreviations
CSU VTH

Colorado State University Veterinary Teaching Hospital

Fab

fragment antigen binding

IQR

interquartile range

NSAID

non-steroidal anti-inflammatory drug

NWC

New World camelids

PT

prothrombin time

PTT

partial thromboplastin time

RR

reference range

Venomous snakes in North America belong to the families Crotalidae and Elapidae. Most snakebites in the United States are because of members of the family Crotalidae.[1] The Crotalidae family includes rattlesnakes, copperheads, and cottonmouths. Approximately 80% of snakebites result in envenomation.[2] Morbidity and case fatality are regionally specific because of variability in relative toxicity of the species of snake encountered. Venom is injected into prey as an aid to immobilization, death, and digestion.[1]

Limited literature exists regarding rattlesnake envenomation of New World camelids (NWC). A previous report of Western diamondback rattlesnake envenomation in NWC from the western coastal United States documented a high mortality rate and guarded prognosis for survival.[3] Encountered snake species vary by region. The prairie rattlesnake (Crotalus viridis viridis) is the only wild venomous snake in northeastern Colorado, and thus the only venomous snake responsible for snakebite envenomation in animals living within approximately a 200-mile radius of the referral hospital in the present study.[4] Species of snake envenomation might predict regional outcomes in NWC.

The purpose of this study was to describe the clinical findings, treatments, and outcomes of NWC after envenomation in the Rocky Mountain region of the United States by prairie rattlesnakes (C. v. viridis). We hypothesized that prairie rattlesnake envenomation of NWC would result in survival rates higher than those reported for rattlesnakes in other regions, and that the survival rate would more closely approximate that for prairie rattlesnake envenomation in other mammalian species.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Acknowledgment
  7. References

A retrospective, computer-generated search of the medical record database of NWC evaluated for rattlesnake envenomation as coded by the attending clinician from 1992 to 2012 at the Colorado State University Veterinary Teaching Hospital (CSU VTH), as well as total numbers of NWC treated during this time period, was performed. Month of admission, signalment, area of bite, clinical signs, clinicopathologic data, treatment, and outcome were recorded. The clinical sign of respiratory distress was defined as nostril flare and audible inspiratory stridor. Fever was defined as rectal body temperature >101.5°F. Tachycardia was defined as a heart rate >90 beats/min and tachypnea as respiratory rate >30 breaths/min.

Statistical analysis was performed using commercial software.1 Continuous data were tested for normality and as most were not normally distributed, reported as median and interquartile range (IQR). Logistic regression was used to evaluate for an association between age, days of hospitalization, and outcome. Fisher's exact test was used to evaluate for an association between platelet count, and treatments of steroids, NSAIDS, and commercial antivenin on outcome. For all comparisons, significance was set at a value of P < .05.

Results

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Acknowledgment
  7. References

Twenty-seven NWCs were evaluated for rattlesnake envenomation at the CSU VTH in this time period, including 25 llamas (Lama glama) and 2 alpacas (Vicugna pacos). Llamas were overrepresented when compared to hospital caseload; during the same time period, a total of 3092 llamas and 2014 alpacas were admitted to the CSU VTH. The NWC evaluated for envenomation ranged in age from 0.5 to 19 years, and the median age at envenomation was 4 years (IQR: 2.0–6.3 years). There were 10 intact males, 9 castrated males, and 8 females. All NWC were evaluated for envenomation between May and October and originated from areas known to be endemic for prairie rattlesnakes (C. v. viridis). All NWC presented with acute manifestations of envenomation, with 26 alive and 1 dead on arrival.

The site of envenomation was identified in 24 cases. The face was the most common site of envenomation (23/24) and 1 NWC was bitten on a hindlimb. Swelling at the region of the bite was noted in all animals. Presenting clinical signs included respiratory distress (11/23), fever (13/23), tachycardia (5/23), and tachypnea (13/23). Based on degree of respiratory distress secondary to envenomation, 2 NWC had a tracheotomy performed before referral and 7 upon CSU VTH presentation. Of the 9 NWC in which a tracheotomy was performed, 3 died, 2 were euthanized, and 4 were discharged alive.

Complete blood count was evaluated upon admission in 20 NWC (see Table 1) and revealed leukocytosis (5/20) and leukopenia (3/20), with most NWC within the normal reference range (RR). Hypoproteinemia was identified in 12/20 NWC. Thrombocytopenia was identified in 11/20 NWC. Echinocytosis was not identified, and hemolysis, detected by hemolytic index, was a consistent finding in NWC with acute rattlesnake envenomation. Serum biochemistry was evaluated upon admission in 17 NWC and revealed hyperglycemia (16/17) with median glucose 294 mg/dL (IQR: 197–415 mg/dL, RR: 90–140 mg/dL), azotemia (6/17) with median creatinine 2.4 mg/dL (IQR: 1.9–3.1 mg/dL, RR: 1.2–2.6 mg/dL), hypoalbuminemia (11/18) with median albumin 3.3 g/dL (IQR: 3.1–3.6 g/dL, RR: 3.5–4.4 g/dL), elevated creatine kinase (7/17) with median creatine kinase 204 IU/L (IQR: 138–894 IU/L, RR: 30–400 IU/L), and elevated aspartate aminotransferase (6/17) with median 215 IU/L (IQR: 156–273 IU/L, RR: 110–250 IU/L). Electrolyte abnormalities included hyponatremia (9/17) with median sodium 147 mEq/L (IQR: 144–150 mEq/L, RR: 147–158 mEq/L), hypokalemia (15/17) with median potassium 3.7 mEq/L (IQR: 3.1–4.2 mEq/L, RR: 4.3–5.6 mEq/L), and hypochloremia (3/17) with median chloride 112 mEq/L (IQR: 108–114 mEq/L, RR: 106–118 mEq/L).

Table 1. Hematology results in 20 New World camelids evaluated for acute prairie rattlesnake envenomation. Results reported as median and interquartile range
TestResultReference Range
Leukocytes16.5 × 103/mL (12.7–19.4 × 103/mL)7.5–21.5 × 103/mL
Neutrophils14.5 × 103/mL (10.2–17.2 × 103/mL)4.6–16.0 × 103/mL
Band neutrophils0 × 103/mL (0–0.2 × 103/mL)0 × 103/mL
Lymphocytes0.8 × 103/mL (0.6–1.4 × 103/mL)1.0–7.5 × 103/mL
Monocytes0.5 × 103/mL (0.3–0.7 × 103/mL)0–0.8 × 103/mL
Platelets126 × 103/mL (54–194 × 103/mL)200–800 × 103/mL
PCV30% (25–33%)29–39%
TP5.2 g/dL (4.8–5.6 g/dL)5.5–7.5 g/dL
Fibrinogen200 mg/dL (100–275 mg/dL)100–400 mg/dL

Of the 26 NWC alive at presentation, 24 were admitted for observation and treatment and 2 were euthanized upon presentation because of severity of clinical signs. Most NWC were treated with intravenous fluids (17), antibiotic treatment (21), and flunixin meglumine NSAID (18). Specific antibiotic treatment consisted of penicillin (13), ceftiofur (19), gentamicin (2), and fluorfenicol (1). Additional treatments included supplemental oxygen (8), corticosteroids (10), antivenin2 (12), plasma (2), and whole blood (1). The most common corticosteroid administered was dexamethasone (9) and 1 animal received prednisolone sodium.

Median duration of hospitalization was 3 days (IQR: 2–5 days). Of the 27 NWC presented to the CSU VTH for snake envenomation, 1 was dead on arrival, 3 died, and 5 were euthanized. Eighteen NWC survived to hospital discharge. Overall, survival rate was 69%. Survivors had longer hospital stays than nonsurvivors (P = .005). Age did not significantly impact outcome (P = .760). Thrombocytopenia identified upon admission did not have a statistically significant association with outcome (P = .618). Treatment with either NSAIDS or corticosteroids was not associated with outcome. Administration of antivenin did not have a statistically significant association with outcome (P = .371). However, 17% mortality was noted with administration of antivenin, and 36% mortality was noted without administration of antivenin.

Discussion

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Acknowledgment
  7. References

This is the first report to describe the clinical findings, treatments, and outcome of NWC with prairie rattlesnake (C. v. viridis) envenomation in the Rocky Mountain region of the United States. The occurrence of snake envenomation of NWC between May and October is consistent with hibernation patterns of prairie rattlesnakes in the Rocky Mountain region. Prairie rattlesnakes typically hibernate from mid-October to late March or early April in this region.[4] The majority of NWC sustained snake bites to the head region, similar to a previous report.[3] Swelling at the site of envenomation commonly resulted in respiratory difficulty, and emergency tracheotomy was required to maintain airway in those most severely affected. Male NWC and llamas (Lama glama) were overrepresented in the present study, perhaps related to husbandry or other exposure variables. In our hospital region, llamas are more likely than alpacas to be housed in the foothills than in the high plains, and live and work in more remote or backcountry areas. In addition, male NWC are thought by some to behave with curiosity or boldness when encountering a threat and when the threat encountered is a rattlesnake, these behavioral traits may in part explain the sex predilection seen in envenomation. The case fatality rate for rattlesnake envenomation of NWC in the Rocky Mountain region in the present study of 31% was lower than that reported in NWC in the Western coastal area. The case fatality rate identified in the present study more closely resembles the case fatality rate in horses with prairie rattlesnake envenomation in the Rocky Mountain region (25%) than that reported in NWC with western diamondback rattlesnake envenomation in the Western coastal United States (58%). This finding is consistent with the hypothesis that this species of snake is highly associated with envenomation outcome. Consistent with other reports from the Rocky Mountain region,[4-6] prairie rattlesnake envenomation may lead to less severe clinical signs of disease and improved outcomes when compared to envenomation with other rattlesnake species.

Clinicopathologic abnormalities commonly encountered were hypoproteinemia, hypoalbuminemia, thrombocytopenia, and hemolysis. Prairie rattlesnake envenomation alters capillary membrane permeability, which can contribute to hypoproteinemia and hypoalbuminemia.[7] Thrombocytopenia is common in humans, horses, and dogs after crotalid envenomation.[1, 4, 8, 9] Although the specific etiology of postenvenomation thrombocytopenia has not been as yet specifically elucidated, a proposed mechanism is venom phospholipase-induced damage to the platelet membranes, which then triggers destruction, initiation of platelet aggregation and consumption at the site of envenomation.[1, 8] Hematologic abnormalities associated with coagulation, including prolonged PT, prolonged PTT, and thrombocytopenia are common after rattlesnake envenomation and result in increased morbidity and mortality.[9] In addition, thrombocytopenia has been shown to be a key factor associated with difficulty in achieving initial control with Crotalidae polyvalent immune Fab antivenom in human snakebite patients.[10] Although in the present study thrombocytopenia was not statistically associated with survival, this study would have required 117 cases to have sufficient power to detect this difference. Hemolysis, consistently identified in the present study, is considered to be an indicator of severe envenomation and results directly from venom-associated erythrocyte membrane damage.[1, 11]

Although frequently used in the present study, systemic antimicrobial treatment after snake envenomation is controversial. Prophylactic administration of antimicrobials is not indicated in humans although there is a risk of bacterial infection associated with snake envenomation when antimicrobials are withheld.[12-15] Prophylactic antimicrobials are used in dogs with snake envenomation.[4, 16] In a study of 100 dogs evaluated for prairie rattlesnake envenomation, 87 dogs were treated with systemic antimicrobials and no wound infections were observed.[4] In 2 studies of horses evaluated for rattlesnake envenomation, 26 of 27 and 57 of 58 horses were treated with systemic antimicrobials, though no beneficial or adverse effects were specifically identified.[6, 8] Systemic antimicrobials were a standard treatment in NWC with rattlesnake envenomation.[4] There are no prospective studies evaluating antimicrobial treatment of domestic animals after snake envenomation to inform treatment decisions in these populations.

Administration of antivenin has been recommended with worsening local injury, clinically significant coagulopathy, or systemic signs of illness after envenomation.[1] It should be administered within 4 hours of envenomation and can have clinically positive effects for up to 24 hours after envenomation. Crotalidae polyvalent immune Fab antivenin is an effective treatment in humans with crotaline envenomation, halting progression of local injury and lessening systemic effects of envenomation.[17] Antivenin2 has been associated with reduced morbidity in dogs after snake envenomation.[18] In the present study, 12 NWC were treated with antivenin and of these, 10 survived to hospital discharge. Although administration of antivenin was not statistically associated with outcome in the present study, a 17% case fatality with administration and 36% without administration was observed. Although further study is warranted, there currently is evidence for antivenin treatment in NWC with acute rattlesnake envenomation.

In conclusion, case fatality rate for prairie rattlesnake envenomation in NWC residing in the Rocky Mountain region was lower than that reported in other regions of the United States, and similar to that reported for prairie rattlesnake envenomation in horses in the same region. Because of the common site of rattlesnake envenomation on the head region of NWC, respiratory distress is a common sequela and emergency tracheotomy to maintain airway is a necessary treatment if severe. Antivenin treatment should be considered in acute envenomation.

Acknowledgment

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Acknowledgment
  7. References

This study was not supported by grant funding. This work was completed at the Colorado State University Veterinary Teaching Hospital.

Conflict of Interest: Authors disclose no conflict of interest.

Footnotes
  1. 1

    STATA 12, StataCorp, College Station, TX

  2. 2

    Antivenin – Crotalidae polyvalent Equine, Wyeth Laboratories, Marietta, PA

References

  1. Top of page
  2. Abstract
  3. Materials and Methods
  4. Results
  5. Discussion
  6. Acknowledgment
  7. References