Twenty alpaca crias (13 females and 7 males) were examined at a university veterinary medical teaching hospital between January 1, 2000, and December 31, 2006, because of diarrhea (n = 20), weight loss (15), and poor appetite (5). Affected crias ranged from 6 to 180 days of age, with 14 crias between 8 and 18 days of age at time of admission. Of the 6 remaining crias, 2 were younger (both were 6 days old at time of admission) and 4 were older (2 were 23 days old, 1 was 27 days old, and 1 was 180 days old at time of admission). Clinical signs were detected by the owners from 6 hours to 14 days before admission, with 15 having clinical signs for 6 hours to 4 days before admission. Seventeen crias were from a single farm. All crias were affected between July and December.
Physical examination revealed that 5 crias had hyperthermia at time of admission, with rectal temperatures of 39.4° to 41.2°C (103.0° to 106.2°F; reference range, 37.5° to 39.2°C [99.5° to 102.5°F]).1 Sixteen crias had tachycardia of 140 to 220 beats/min (reference range, 60 to 120 beats/min).1 Eleven crias had tachypnea of 40 to 90 breaths/min (reference range, 10 to 30 breaths/min).1 Rectal temperatures, heart rates, and respiratory rates of the remaining crias were within the respective reference ranges.
All crias had diarrhea and staining of the perineum. Diarrhea ranged from a milky white to a more normal tan color, and green fecal material was evident in crias that were old enough to forage. Consistency was watery in the most severely affected crias or pasty in the moderately affected crias. Three crias were obtund at admission and severely dehydrated with sunken eyes, dry mucous membranes, and signs of hemodynamic shock. Eight crias were quiet and not suckling well, with various degrees of dehydration. The remaining 9 crias appeared bright and alert.
Cryptosporidiosis was diagnosed in each of the 20 crias on the basis of microscopic identification of the organism in feces by use of acid-fast staining with confirmatory fluorescent antibody staining.a Feces from 4 dams of the crias were tested by use of the same methods, and all 4 had negative results for cryptosporidia. Four crias also had Giardia organisms as determined on the basis of microscopic analysis of wet mounts, which was confirmed with fluorescent antibody staining.b Electron microscopy revealed coronavirus infection in 2 crias. Additionally, fecal evaluation by use of a flotation technique revealed that several crias were also parasitized by tapeworms, coccidia, and strongyles (Table 1). Thirteen crias had no other potential gastrointestinal tract pathogens (other than Cryptosporidium organisms) identified during fecal examination by use of any of the techniques.
Concurrent potential pathogens identified by use of various techniques in the feces of 20 alpaca crias with diarrhea and Cryptosporidium infection.
| No. of crias | Flotation method | Wet mount | Electron microscopy | Microbial culture |
|---|---|---|---|---|
| 1* | Coccidia and strongyles | Giardia spp | Negative | Negative |
| 1* | Negative | Giardia spp | Coronavirus | Negative |
| 1 | Negative | Negative | Coronavirus | Negative |
| 1 | Tapeworms | Negative | Negative | Negative |
| 1 | Coccidia | Negative | Negative | Negative |
| 2 | Negative | Giardia spp | Negative | Negative |
| 13† | Negative | Negative | Negative |
Cria did not survive until discharge from the hospital.
Two crias did not survive until discharge from the hospital.
Blood gas analyses were performed on venous samples obtained at the time of admission (Table 2). Eleven crias had acidemia (pH, < 7.35). Four crias with acidemia had evidence of mixed acid-base disorders with bicarbonate concentrations within or greater than the reference range (reference range, 26 to 28 mmol/L) but no other metabolic abnormalities, which suggested that respiratory acidosis may have been a factor. This could not be determined because blood gas analysis was not routinely performed on arterial blood samples at time of admission.
Serum biochemical and hematologic results for samples obtained at time of admission from 20 crias with cryptosporidiosis.
| Variable | Reference range | Less than reference range | Within reference reference range | Greater than reference range |
|---|---|---|---|---|
| pH (19) | 7.35–7.45 | 11 | 8 | 0 |
| Bicarbonate (19) | 24–26 (mmol/L) | 7 | 8 | 4 |
| Anion gap (20) | 2–18 (mEq/L) | 0 | 13 | 7 |
| Sodium (20) | 146–156 (mEq/L) | 6 | 8 | 6 |
| Chloride (20) | 109–125 (mEq/L) | 5 | 8 | 7 |
| Potassium (20) | 3.8–7.3 (mEq/L) | 5 | 15 | 0 |
| Ionized calcium (20) | 4.5–5.5 (mg/dL) | 1 | 19 | 0 |
| Lactate (17) | 0.5–2.0 (mmol/L) | 0 | 7 | 10 |
| Glucose (20) | 80–132 (mg/dL) | 0 | 6 | 14 |
| PCV (20) | 25–33 (%) | 1 | 11 | 8 |
| Total protein (20) | 5–6 (g/dL) | 6 | 9 | 5 |
| Albumin (18) | 3.5–4.9 (g/dL) | 13 | 5 | 0 |
| Globulin (18) | 1.2–3.4 (g/dL) | 0 | 14 | 4 |
| SUN (20) | 13–28 (mg/d) | 0 | 9 | 11 |
| Creatinine (20) | 0.9–1.7 (mg/dL) | 2 | 12 | 6 |
| Total bilirubin (18) | 0.1–0.2 (mg/dL) | 0 | 10 | 8 |
| AST (17) | 127–298 (U/L) | 0 | 5 | 12 |
| GGT (18) | 10–37 (U/L) | 1 | 6 | 11 |
| SDH (7) | 1.5–15.7 (U/L) | 0 | 4 | 3 |
| CK (17) | 43–750 (U/L) | 0 | 16 | 1 |
| WBCs (18) | 8.0 × 103–21.4 × 103 (WBCs/μL) | 3 | 13 | 2 |
| Platelets (17) | 2 × 105–4 × 105 (cells/μL) | 1 | 11 | 5 |
Numbers in parentheses indicate number of crias from which samples were obtained.
AST = Aspartate transaminase. GGT = γ-Glutamyltransferase. SDH = Sorbitol dehydrogenase. CK = Creatine kinase.
Serum biochemical analyses and CBCs were performed within 24 hours after admission (Table 2). Approximately a third of the crias had hyponatremia and hypochloremia, and another third had hypernatremia and hyperchloremia. Of the 6 crias with hypernatremia, 4 had sodium concentrations > 170 mEq/L. The 4 crias with sodium concentrations > 170 mEq/L also had chloride concentrations > 140 mEq/L and glucose concentrations > 300 mg/dL, which was suggestive of hyperosmolar disorder.2 Other common abnormalities identified in crias with cryptosporidiosis included hypokalemia, hyperlactemia, hyperglycemia, hypoalbuminemia, azotemia, hyperbilirubinemia, a high PCV, and high serum activities of aspartate transaminase and γ-glutamyltransferase.
The IgG concentration was measured in only 6 of 20 crias on the day of admission. Use of radial immunodiffusion assay revealed that 5 crias had adequate IgG concentrations (> 800 mg/dL), but the IgG concentration in 1 cria was only 450 mg/dL. No other specific measures of immune function were performed.
Whereas all of the crias were judged to have enterocolitis as the primary disease, some of the crias had additional problems that could have been related to Cryptosporidium infection. Blood samples were obtained for microbial culture from 14 crias, and 2 cultures yielded growth (both were Pseudomonas spp). Two crias had corneal ulcers and conjunctivitis, and 3 crias had metabolic acidosis, severe azotemia, and inadequate urine production. Those 3 crias also subsequently developed seizures that were refractory to treatment.
Nineteen crias were hospitalized. Median duration of hospitalization was 7 days (range, 0 to 25 days). Eleven crias received oral supplementation of nutrients consisting of goat milk or kid milk replacer (approx 9% of body weight/d). Of the 13 crias for which body weight was obtained at admission and discharge, all of those that survived until discharge gained between 0.45 and 0.91 kg (1 and 2 lb) during hospitalization. All of the crias that did not survive lost weight during hospitalization, despite oral and parenteral administration of nutrients.
All hospitalized crias were treated by IV administration of fluids (50 mL/kg/d [22.7 mL/lb/d]). Most of the crias received supplemental amino acids, dextrose, B vitamins, potassium, and calcium in the fluids. One cria was treated by use of total parenteral administration of nutrients. Nine received insulin to address hyperglycemia, an increase in E-hydroxybutyrate concentrations, or an increase in concentrations of nonesterified fatty acids, which were monitored throughout hospitalization. Ten received at least 1 plasma transfusion (approx 300 mL/cria) with hyperimmunized llama plasma,c and 1 additional cria received a synthetic colloid.d Nineteen crias were administered antimicrobials (ceftiofur sodium or a combination of penicillin-amikacin or penicillin-gentamicin). Two crias received azithromycin. Other supportive treatments included a gastroprotectant (sucralfate), an anti-inflammatory (flunixin meglumine), antiparasitic compounds (amprolium, ivermectin, metronidazole, or sulfadimethoxinee), supplemental vitamins or trace minerals (thiamine, vitamin E, and seleniumf), a topically applied antimicrobial ophthalmic ointment,g or antidiarrheic agents (smectite earth,h a probiotic,i and bismuth subsalicylicate) on the basis of the perceived need of each cria or the clinical discretion of the attending veterinarian.
The 3 crias with inadequate urine production and severe azotemia were treated with furosemide administered IV as a bolus or as a constant rate infusion. These crias also were administered fluids at a higher rate, which ranged from 100 to 300 mL/kg/d (45.5 to 136.4 mL/lb/d). These same 3 crias were administered a combination of mannitol, diazepam, and phenobarbital to ameliorate seizures.
The 3 crias with inadequate urine production, severe azotemia, and refractory seizures died or were euthanatized. One intensively managed cria with unresolving diarrhea of several weeks' duration was euthanatized, and necropsy of that cria revealed hepatic necrosis and evidence of vitamin E deficiency and nutritional secondary hyperparathyroidism. Another cria recovered from the diarrheic condition and was discharged from the hospital; however, several weeks later, that cria was readmitted because of severe ataxia. Cause of the ataxia was identified as an abscess in a cervical vertebra, and the cria was subsequently euthanatized. We did not believe the cria's death was directly attributable to cryptosporidiosis, and that cria was included in the survivors.
Data obtained at the time of admission were compared between survivors and nonsurvivors (Table 3). All nonsurvivors lost weight during hospitalization, whereas all survivors gained weight during hospitalization. Cost of treatment was not a consideration in outcome for the nonsurvivors.
Comparison of medical history and clinical fndings between surviving and nonsurviving crias with Cryptosporidium infection.
| Variable | Survivors (n = 16)* | |
|---|---|---|
| Received azithromycin | 0/16 | 2/4 |
| Weight loss | 0/9 | 4/4 |
| Metabolic acidosis at time of admission | 8/16 | 3/4 |
| Hyperosmolar syndrome | 3/16 | 1/4 |
| Duration of hospitalization (d) | 10 × 4† | 11 × 6† |
| Persistent azotemia | 0/16 | 3/4 |
| Leukopenia | 2/14 | 0/4 |
| Hyperlactemia | 6/12 | 4/4 |
| Hyperbilirubinemia | 6/14 | 2/4 |
| Hypernatremia | 4/16 | 1/4 |
| Hyponatremia | 6/16 | 0/4 |
| High activities of liver enzymes | 8/12 | 4/4 |
| Coronavirus† | 1/16 | 1/4 |
| Giardia spp† | 1/16 | 2/4 |
| Adequate serum IgG concentrations§ | 4/5 | 1/1 |
| Fed by use of a tube | 7/16 | 4/4 |
| Bacteremia | 2/11 | 0/3 |
Survivors were crias that were discharged from the hospital, whereas nonsurvivors were crias that died or were euthanatized and thus were not discharged from the hospital. Values reported are number of crias with the result/number of crias tested.
Value reported is mean × SD.
DOrganisms were detected during microbial culture of fecal samples.
Concentration > 800 mg/dL, as determined by use of a radial immunodiffusion assay.
Discussion
Analysis of the data reported here suggested that Cryptosporidium organisms were important enteric pathogens or copathogens in crias (especially crias < 3 weeks old) and that Cryptosporidium infection can become endemic on some farms. Clinical signs often were evident for 7 or more days; however, with supportive care, most had self-limiting infections. Crias up to 6 months of age had cryptosporidiosis and diarrhea, but testing of 4 dams of Cryptosporidium-shedding crias did not detect infections in the adult alpacas. Furthermore, the authors are not aware of any published reports of camelids > 6 months old in which cryptosporidiosis has been confirmed.
In 13 crias, no other potential pathogen was identified. This supports the role of Cryptosporidium sp as a primary pathogen. Giardia organisms were the most common concurrently isolated pathogen. Giardiasis has been reported in combination with cryptosporidiosis in goat kids,3 baby pigs,4 and calves,4 and the same association may hold true in crias. Considering that Giardia organisms are also commonly isolated from crias with diarrhea,5 coisolation may have been a coincidence. Bacteremia was a complication associated with cryptosporidiosis in 2 crias. Although Pseudomonas sp has been infrequently reported as a cause of sepsis in crias,6 it is not commonly associated with diarrhea. This would suggest that the bacteremia was likely secondary to cryptosporidiosis, whereas some of the enteric parasites and viruses may have acted as copathogens.
All of the crias were admitted in late summer, fall, or early winter to the veterinary medical teaching hospital, which is located in the Pacific Northwest. The temporal nature of these infections may have been influenced by an outbreak on a single farm and therefore should be interpreted with caution. This time of year also corresponds to the period of neonatal susceptibility after the spring and fall birthing seasons. Cryptosporidiosis in camelids has been reported in February (United Kingdom)7 and in July, October, and February (Pacific Northwest).5 In calves, the highest prevalence of the disease is during the summer months.8 This information likely indicates that Cryptosporidium infection can develop in animals in temperate climates throughout the year.
Many of the affected crias had hyperglycemia and high activities of liver enzymes. These abnormalities could have resulted from stress and a subsequent inability to use glucose, with secondary hepatic lipidosis. The high activities of liver enzymes also may have resulted from sepsis or inadequate perfusion of hepatic tissue. Metabolic acidemia and electrolyte abnormalities are generally milder or less common in crias than in other neonatal ruminants with cryptosporidiosis.9 Another interesting finding was that some crias had hypernatremia, which is an uncommon finding in neonatal calves with diarrhea unless those calves have been orally administered concentrated electrolytes.10 Hypernatremia likely stems from renal water loss during glycuresis or sodium loss because of renal insufficiency. Concurrent sodium retention may contribute. Hypernatremia has been reported2 in camelids, and camelids appear to be prone to develop hypernatremia in a number of disease states.11 Considering that camelids may be prone to developing hypernatremia, electrolyte patterns can be varied in crias with cryptosporidiosis, and the importance of establishing the status of renal function in ill crias underscores the value of obtaining samples for serum biochemical analyses at the time of admission.
Although neurologic abnormalities, persistent azotemia, and hyperthermia are not typically detected in neonatal ruminants with cryptosporidiosis, they were evident with some frequency (3/20) in the alpaca crias reported here. It is possible that the neurologic signs were the result of cerebral edema or cerebral dehydration that resulted from profound hypernatremia, or they may possibly have been caused by renal encephalopathy. Often, Cryptosporidium-infected calves have hypothermia with severe dehydration and diarrhea,10 but the crias reported here more commonly had hyperthermia, which could have been attributable to severe inflammation resulting from enteritis. Persistent azotemia despite fluid administration was presumed to be a result of renal insufficiency, which may have been secondary to severe dehydration. This is a relatively uncommon finding in calves with severe dehydration as a result of diarrhea.12 It is possible that camelids are more prone to renal insufficiency as a result of severe dehydration than other neonatal ruminants.
Crias with azotemia that did not respond to aggressive fluid administration and crias with weight loss despite tube feeding had a poor outcome. Bacteremia and hyperosmolar syndrome did not appear to be linked to fatalities, which indicated that they are treatable disorders. The high rate of antimicrobial use in these crias reflected concerns about bacteremia, which is a complication that has been identified in camelids with parasitic enteritis.13 The fact that all crias that received azithromycin died or were euthanatized was likely attributable to the fact that the only animals administered azithromycin were those that failed to respond to supportive care and therefore had much more severe disease and secondary complications.
Cryptosporidiosis has been reported5,7,14–16 in only 15 New World camelids. Cryptosporidiosis was diagnosed in 5 camelids during necropsy performed after they had diarrhea, deteriorated rapidly, and died.7,14 Cryptosporidiosis was identified in 4 crias during a study5 on causes of diarrhea in unweaned crias and in 5 crias in a study16 on an outbreak of diarrhea at an alpaca breeding farm; 1 case of cryptosporidiosis was an intensively managed cria with chronic diarrhea.15 Analysis of our data suggests that the disease may be more widespread than previously recognized, particularly in certain herds, and that early institution of treatment may result in a favorable outcome. Risk factors for camelid herds have not yet been evaluated. In cattle, a high density of young, susceptible calves is likely to increase risk of infection,8 and it is likely that a similar risk factor would be expected for alpacas. The farm that accounted for the majority (17/20) of crias in our report was a small property (2 hectares [5 acres]) that housed at least 50 crias/y.
Cryptosporidiosis should be considered as a cause of diarrhea in alpaca crias (up to 6 months of age). Including cryptosporidiosis in the list of differential diagnoses is also valuable from a client-communication standpoint to raise the awareness of its zoonotic potential.16 Supportive care appears to be important for a successful outcome, which was achieved in 16 of 20 infected crias in this report.
TB Auramine M acid-fast and fluorescent antibody stain, Becton-Dickinson, Sparks, Md.
Giardi-a-Glo (ST102R), Waterborne Inc, New Orleans, La.
Triple J Farms, Bellingham, Wash.
Hespan (hetastarch 6%/0.9% NaCl), 500 mL, Hospira Inc, Lake Forest, Ill.
Albon, Pfizer Animal Health, Exton, Pa.
BoSe, Schering-Plough Animal Health Corp, Union, NJ.
Neomycin and Polymyxin B Sulfates and Bacitracin Zinc Ophthalmic Ointment USP, Bausch & Lomb Inc, Meridian, Idaho.
BioSponge, Platinum Performance, Buellton, Calif.
Probios, Vets Plus Inc, Knapp, Wis.
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