Between October 1, 2002, and January 1, 2006, 15 llamas and 34 alpacas that were admitted to the Oregon State University Veterinary Teaching Hospital or submitted in whole or in part to the Oregon State University Veterinary Diagnostic Laboratory were found to have fecal oocysts or intestinal coccidial stages morphologically consistent with Eimeria macusaniensis. Of the 44 camelids for which age was recorded, 13 were between 3 weeks and 7 months old, 9 were between 1 and 3 years old, 5 were between 3 and 5 years old, and 17 were between 6 and 18 years old. Thirty-three were female, and 14 were male. These camelids represented 5.5% of all camelids admitted to the Veterinary Teaching Hospital, 8.6% of all camelid carcasses submitted to the Veterinary Diagnostic Laboratory for necropsy, and 0.4% of all camelid tissue samples submitted for histologic evaluation during this 39-month period. Sex and age distributions for these 49 camelids were not significantly (χ2 test; P = 0.108 and 0.254, respectively) different from distributions for the general hospital population during this period. Infected camelids came from 29 herds.
Ten llamas and 9 alpacas were submitted in whole or in part to the Veterinary Diagnostic Laboratory for postmortem examination. Of these, 7 were reported to have been found dead. The most common owner complaints for the remaining 12 were weight loss (n = 5), increased recumbency (5), decreased appetite (5), diarrhea (4), a recent history of transport (3), and lethargy (3). Other complaints included suspected transient choke (n = 1) and drooling of clear saliva (1). Three of the 4 camelids with diarrhea were the youngest of these 19 camelids; all 3 were < 1 year old.
Five llamas and 25 alpacas were admitted to the Veterinary Teaching Hospital. Common owner complaints and physical examination findings were lethargy (n = 15), weight loss (14), diarrhea (14), decreased appetite (13), a recent history of transport (11), increased recumbency (8), seizures or other neurologic signs (5), colic (4), and dyspnea (4). Also identified were abdominal distention (n = 3), salivary loss (2), dysphagia (1), a putrid oral odor (1), a heart murmur (1), and a stiff gait (1). Lethargy, decreased appetite, or weakness were the major complaints in 20 of the 30 camelids admitted to the Veterinary Teaching Hospital, diarrhea was the major complaint in 6, and colic was the major complaint in 1. The remaining 3 camelids were examined because of a fracture, dysphagia, and E macusaniensis infection identified by the referring veterinarian. Five of the 14 camelids with diarrhea were < 18 months old, and 7 of the 14 came from a single herd. Reported duration of clinical signs ranged from < 1 day to 1 month, but generally, camelids were reported to have been doing well until 1 to 3 days prior to admission. Once signs were noticed, rapid progression was common, except that diarrhea often resolved despite worsening of other signs. In 4 camelids, clinical signs were generally mild from the start and never worsened.
Heart rate was > 72 beats/min on initial examination in 14 of the 30 camelids admitted to the Veterinary Teaching Hospital, 10 of which subsequently died. Rectal temperature was < 37.5°C (99.5°F) in 14 camelids, 11 of which subsequently died, and > 39.2°C (102.5°F) in 1. Respiratory rate was > 30 breaths/min in 6 camelids, 5 of which subsequently died. Fifteen of the 30 camelids admitted to the Veterinary Teaching Hospital survived to discharge.
Blood analyses were performed at the time of admission in 29 of the 30 hospitalized camelids (Tables 1 and 2). The most common biochemical abnormalities were high nonesterified fatty acid concentrations (13/16), hypoalbuminemia (20/25), hypoproteinemia (21/29), high aspartate aminotransferase activity (16/23), hypokalemia (17/27), hyperglycemia (17/28), hyperketonemia (9/16), hyponatremia (14/28), and hyperlactemia (10/21). Common hematologic abnormalities were leukocytosis (7/22), neutrophilia (7/18), high band neutrophil count (14/19), monocytosis (6/19), and eosinopenia (15/19). The RBC count was within reference limits in 15 of 18 camelids, but 5 of 18 camelids had low hemoglobin concentration, and 9 of 29 had low PCV.
Results of biochemical analyses performed in llamas and infected with Eimeria macusaniensis.
| Variable | No. of camelids (No. that did not survive) | ||
|---|---|---|---|
| No. with value < lower reference limit | No. with value within reference limit | No. with value > upper reference limit | |
| pH | 5 (5) | 14 (8) | 2 (1) |
| Total CO2 | 11 (7) | 7 (3) | 9 (4) |
| Sodium | 14 (7) | 14 (7) | 0 (0) |
| Potassium | 17 (7) | 10 (6) | 0 (0) |
| Chloride | 11 (7) | 15 (6) | 1 (1) |
| Ionized calcium | 10 (7) | 10 (7) | 0 (0) |
| Total calcium | 9 (2) | 9 (6) | 2 (1) |
| Anion gap | 10 (2) | 11 (5) | 7 (7) |
| Glucose | 5 (5) | 6 (2) | 17 (7) |
| Lactate | 0 (0) | 11 (5) | 10 (8) |
| Urea nitrogen | 4 (1) | 13 (6) | 8 (6) |
| Creatinine | 2 (1) | 13 (3) | 10 (9) |
| Plasma protein | 21 (11) | 6 (2) | 2 (2) |
| Serum protein | 15 (6) | 4 (2) | 0 (0) |
| Albumin | 20 (10) | 5 (3) | 0 (0) |
| Cholesterol | 6 (3) | 6 (2) | 4 (3) |
| Triglyceride | 0 (0) | 12 (5) | 4 (3) |
| BOHB | 0 (0) | 7 (4) | 9 (3) |
| NEFA | 0 (0) | 3 (3) | 13 (4) |
| Creatine kinase | 0 (0) | 19 (8) | 4 (3) |
| GGT | 1 (0) | 12 (5) | 11 (7) |
| AST | 1 (0) | 6 (1) | 16 (10) |
| SDH | 0 (0) | 14 (5) | 3 (2) |
| Phosphorus | 4 (1) | 10 (3) | 4 (4) |
| Magnesium | 1 (0) | 14 (6) | 2 (2) |
BOHB = β-Hydroxybutyrate. NEFA = Nonesterified fatty acids. GGT = γ-Glutamyl transferase. AST = Aspartate aminotransferase. SDH = Sorbitol dehydrogenase.
Results of hematologic analyses performed in llamas and alpacas infected with E macusaniensis.
| Variable | No. of camelids (No. that did not survive) | ||
|---|---|---|---|
| No. with value < lower reference limit | No. with value within reference limit | No. with value > upper reference limit | |
| WBC count | 1 (1) | 14 (8) | 7 (4) |
| Neutrophil count | 3 (1) | 8 (4) | 7 (4) |
| Band neutrophil count | 0 (0) | 5 (2) | 14 (7) |
| Lymphocyte count | 0 (0) | 16 (7) | 3 (2) |
| Monocyte count | 0 (0) | 13 (6) | 6 (3) |
| Eosinophil count | 15 (8) | 4 (1) | 0 (0) |
| RBC count | 0 (0) | 15 (5) | 3 (3) |
| Hemoglobin | 5 (2) | 13 (6) | 0 (0) |
| PCV | 9 (4) | 20 (11) | 0 (0) |
| MCH | 9 (4) | 9 (4) | 0 (0) |
| Fibrinogen | 0 (0) | 20 (10) | 1 (0) |
MCH = Mean corpuscular hemoglobin.
The Mann-Whitney rank sum test was used to compare physical examination, hematologic, and biochemical findings between camelids that survived and those that died or were euthanized (Table 3). Surviving camelids were found to have significantly lower heart rates; anion gap; PCV; serum hemoglobin, urea nitrogen, creatinine, and total bilirubin concentrations; and serum creatine kinase and G-glutamyl transferase activities and significantly higher rectal temperatures than nonsurviving camelids. Other physical examination, hematologic, and biochemical findings were not significantly different between surviving and nonsurviving camelids.
Comparison of selected physical, biochemical, and hematologic findings in llamas and alpacas with E macusaniensis infection that did or did not survive.
| Variable | Survivors | Nonsurvivors | P value* | Reference range |
|---|---|---|---|---|
| Heart rate (beats/min) | 66 (60–80) n = 13 | 96 (71–119) n = 15 | 0.009 | 48–80 |
| Rectal temperature (°C) | 38.3 (37.6–38.90) n = 14 | 37.1 (34.6–37.8) n = 15 | 0.002 | NA |
| Anion gap (mEq/L) | 12.7 (11.3–15.2) n = 14 | 22.0 (12.3–28.7) n = 14 | 0.014 | 15–27 |
| BUN (mg/dL) | 18.0 (12.8–23.0) n = 13 | 27.6 (20.4–48.0) n = 13 | 0.021 | 13–28 |
| Creatinine (mg/dL) | 1.2 (1.0–1.4) n = 13 | 2.3 (1.3–3.8) n = 13 | 0.013 | 0.9–1.7 |
| Bilirubin (mg/dL) | 0.10 (0.10–0.20) n = 13 | 0.25 (0.15–0.40) n = 8 | 0.027 | < 0.4 |
| Creatine kinase (U/L) | 128 (75–205) n = 13 | 265 (206–1,468) n = 10 | 0.014 | 43–750 |
| GGT (U/L) | 15 (11–43) n = 13 | 52 (15–78) n = 12 | 0.050 | 10–37 |
| PCV (%) | 28 (24–30) n = 14 | 32 (27–35) n = 15 | 0.022 | 27–45 |
| Hemoglobin (g/dL) | 12.6 (10.9–14.0) n = 11 | 15.9 (12.5–16.1) n = 7 | 0.046 | 11.9–19.4 |
Data are given as median (interquartile [25th to 75th percentile] range).
Mann-Whitney rank sum test.
NA = Not applicable. To convert degrees Celsius to Fahrenheit, multiply by 9/5 and add 32.
See Table 1 for remainder of key.
Feces (n = 7), blood (5), liver biopsy specimens (3), and peritoneal fluid (2) collected prior to death from select camelids were submitted for bacterial culture. General bacterial culture techniques were used for all samples, except that culture techniques specific for identification of salmonellae and clostridia were used on fecal samples. Bacterial culture of one of the blood samples yielded Escherichia coli, and culture of another blood sample yielded Corynebacterium spp. Bacterial culture of one of the liver biopsy specimens yielded Acinetobacter spp, and culture of one of the fecal samples yielded a heavy growth of Clostridium perfringens.
Postmortem specimens submitted for bacterial culture included intestinal tissue or contents (n = 12), mesenteric lymph nodes (10), liver (8), lung (4), feces (2), and peritoneal fluid (1). General bacterial culture techniques were used for liver, lung, and peritoneal fluid specimens, whereas culture techniques specific for identification of salmonellae and clostridia were used on intestinal, mesenteric lymph node, and fecal specimens. Liver specimens from 2 llamas yielded E coli, a liver specimen from 1 camelid and a lung specimen from another camelid yielded β-hemolytic Streptococcus spp, a lung specimen yielded a mixed population of gram-negative bacteria, an intestinal specimen yielded Clostridium spp, and a mesenteric lymph node specimen yielded group B Salmonella spp.
Feces or intestinal contents were collected within 24 hours of admission or necropsy from 42 of the camelids. No E macusaniensis oocysts were seen in samples from 17 camelids, 1 to 100 oocysts/g were seen in samples from 11 camelids, 101 to 250 oocysts/g were seen in samples from 7 camelids, 251 to 500 oocysts/g were seen in samples from 3 camelids, and > 500 oocysts/g were seen in samples from 4 camelids. The examination technique involved mixing 4 g of solid feces or intestinal contents or 4 mL of liquid feces or intestinal contents with 26 mL of a saturated saline solution (specific gravity, 1.202), straining the mixture through gauze, and loading the strained mixture onto a McMaster counting chamber. Because previous experiences with this parasite had revealed poor flotation in saturated saline solutions, the sample was allowed to sit in the chamber for 15 minutes before counting and the microscope was focused on both the surface and floor of the counting chamber. Additionally, direct smears of feces were examined, and oocysts were seen in samples from 1 additional alpaca for which results of the modified McMaster test had been negative. Examination of follow-up fecal samples collected from 2 alpacas that initially had negative McMaster test results revealed oocysts, with oocyst count peaking at 7,500 oocyst/g 1 week after admission in 1 of the 2 alpacas. For the other alpaca, results were not positive until the fourth sample, which was collected 10 days after admission, was examined. In all cases, the size and shape of the oocysts were considered diagnostic for E macusaniensis1 (Figure 1).
Other potential pathogens isolated from the feces of infected camelids included small coccidia (Eimeria lamae, Eimeria alpacae, or Eimeria punoensis; all < 45 μm in maximum length; n = 17); strongyle ova (13); coronavirus (3); Cryptosporidium spp, Trichuris spp, Capillaria spp, and Giardia spp (2 each); and Nematodirus spp (1). In only 10 of the 42 samples were > 400 nematode ova or small coccidia oocysts found, and in 15 of the 42 samples, no potential pathogens beside E macusaniensis were found.
In camelids in which results of fecal examinations for E macusaniensis were negative, infection was confirmed by means of histologic examination of intestinal tissue. In all but 1 case, intestinal specimens were collected postmortem. In 1 alpaca, jejunal biopsy specimens were obtained during abdominal exploratory surgery performed because of signs of colic, and organisms were identified during cytologic examination of impression smears (Figure 2) as well as during histologic examination of frozen tissue sections. Results of modified McMaster tests performed on fecal samples from this alpaca subsequently became positive.
Photomicrograph of an unsporulated Eimeria macusaniensis oocyst isolated from the feces on an infected camelid. Bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of an unsporulated Eimeria macusaniensis oocyst isolated from the feces on an infected camelid. Bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of an unsporulated Eimeria macusaniensis oocyst isolated from the feces on an infected camelid. Bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
In total, intestinal specimens from 34 camelids were examined. Multiple sections of small intestine were available from all but 5 of the 34. Eimeria macusaniensis was identified on the basis of its characteristic size and appearance, including meronts > 100 μm long; macrogamonts with prominent wall-forming bodies; and maturing oocysts with the characteristic size, shape, and appearance.2 Larger parasitophorus vacuoles; the absence of maturing macrogamonts; and grossly disproportionate numbers of meronts, compared with macrogamonts, aided in the differentiation of meronts from microgamonts in some camelids. When few to moderate numbers of parasites were identified, they were localized near the base of the villi, but in heavily parasitized camelids, the entire villus was affected. Occasional forms appeared to be in the lamina propria. Lesions were most severe in specimens from the ileum and distal portion of the jejunum. Lesions were rarely seen in colonic specimens. When multiple sections of jejunum were available, it was common for some to contain no or few parasites and others to have complete obliteration of the mucosa. Rarely, gross thickening or serosal cobblestoning of the intestine or punctate, white, plaque like mucosal lesions were seen. Examination of impression smears of intestinal mucosa from 1 alpaca revealed high numbers of organisms (several hundred per slide) in the region of plaques and far fewer (3 to 4/slide) in grossly normal adjacent regions of the jejunum and ileum. In some camelids, multiple stages, including mature oocysts, were found, suggesting ongoing exposure for at least 30 days (Figure 3).
Photomicrograph of an impression smear of a jejunal biopsy specimen from an alpaca with prepatent E macusaniensis infection. Notice the epithelial cell nuclei (arrows) displaced by parasitophorus vacuoles (E). A single macrogamont with wallforming bodies (W) is present. Wright stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of an impression smear of a jejunal biopsy specimen from an alpaca with prepatent E macusaniensis infection. Notice the epithelial cell nuclei (arrows) displaced by parasitophorus vacuoles (E). A single macrogamont with wallforming bodies (W) is present. Wright stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of an impression smear of a jejunal biopsy specimen from an alpaca with prepatent E macusaniensis infection. Notice the epithelial cell nuclei (arrows) displaced by parasitophorus vacuoles (E). A single macrogamont with wallforming bodies (W) is present. Wright stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of a section of jejunum from an adult alpaca infected with E macusaniensis. Notice the presence of different stages of the organism, including a microgamont (M), meront (Me), early-stage macrogamont (Mg), macrogamont with distinct wall-forming bodies (W), and oocyst (O). The alpaca was from a farm with a history of E macusaniensis infection. H&E stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of a section of jejunum from an adult alpaca infected with E macusaniensis. Notice the presence of different stages of the organism, including a microgamont (M), meront (Me), early-stage macrogamont (Mg), macrogamont with distinct wall-forming bodies (W), and oocyst (O). The alpaca was from a farm with a history of E macusaniensis infection. H&E stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of a section of jejunum from an adult alpaca infected with E macusaniensis. Notice the presence of different stages of the organism, including a microgamont (M), meront (Me), early-stage macrogamont (Mg), macrogamont with distinct wall-forming bodies (W), and oocyst (O). The alpaca was from a farm with a history of E macusaniensis infection. H&E stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of a section of jejunum from an adult alpaca infected with E macusaniensis. The alpaca had been moved to a new farm 20 days previously, and results of fecal flotation tests were negative. Notice the uniform population of early macrogamonts. H&E stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of a section of jejunum from an adult alpaca infected with E macusaniensis. The alpaca had been moved to a new farm 20 days previously, and results of fecal flotation tests were negative. Notice the uniform population of early macrogamonts. H&E stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Photomicrograph of a section of jejunum from an adult alpaca infected with E macusaniensis. The alpaca had been moved to a new farm 20 days previously, and results of fecal flotation tests were negative. Notice the uniform population of early macrogamonts. H&E stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 1; 10.2460/javma.230.1.94
Examination of tissue specimens from 10 camelids for which results of fecal examinations were positive revealed early gametocytes in 6, gametocytes with distinct wall-forming bodies in 5, mature gametocytes in 4, and oocysts in 4. Examination of tissue sections from 13 camelids for which results of fecal examination were negative for E macusaniensis revealed early gametocytes in 9, gametocytes with distinct wall-forming bodies in 6, mature gametocytes in none, and oocysts in 1 (Figure 4). In 3 of these 13 camelids, only a uniform, mucosa-obliterating population of meronts or early macrogamonts was seen, suggesting recent exposure.
Other lesions identified or confirmed during postmortem examination included hepatic lipidosis (n = 10), pulmonary edema (4), evidence of sepsis (4), gastric ulceration (2), forestomach acidosis (1), colonic feed impaction (1), biliary carcinoma (1), perforation of the colon (1), polioencephalomalacia (1), and glossitis (1). The camelid with polioencephalomalacia had not been treated prior to admission and died within 90 minutes of admission. Severe parasitism by small coccidia was identified in only 2 camelids. Altogether, lesions caused by E macusaniensis appeared to be the primary or most important lesion in at least 11 of the 19 camelids submitted to the Veterinary Diagnostic Laboratory and in 25 of the 30 camelids admitted to the Veterinary Teaching Hospital.
Fifteen camelids were involved in outbreaks of eimeriosis on 4 farms. These farms reported 5 to 20 deaths over periods ranging from 1 week to 3 months, usually in association with a variety of postmortem diagnoses, including hepatic lipidosis, gastric ulceration, and other forms of endoparasitism. For all but 1 farm, multiple cases of E macusaniensis infection were confirmed. In the most severe outbreak, a group of 30 alpacas was transported in late summer to a new farm and placed on a pasture that had been vacant for 6 months. The first death occurred 20 days after the move, and severe prepatent E macusaniensis meront infection was confirmed histologically. Despite treatment of the entire herd with amprolium hydrochloride, an additional 6 alpacas became ill within 13 days, 4 of which died or were euthanized. Two of the 4 that died were determined by means of histologic examination to have had prepatent infections. The two survivors eventually had positive fecal test results. Results of modified McMaster tests performed at Oregon State University on 6 fecal samples obtained from 3 alpacas in this herd within 33 days of the move were all negative for E macusaniensis. Five other alpacas developed lethargy, diarrhea, and inappetance and were found to have patent infections approximately 37 days after the move. Results of modified McMaster tests performed at Oregon State University on fecal samples obtained from 6 alpacas in this herd 37 or more days after the move were all positive, but oocyst count was never > 375/g. No other cause of illness was identified in the alpacas that sickened or died in this herd. Resident alpacas moved to the same pasture at the same time appeared healthy and were not tested at the Veterinary Teaching Hospital.
Treatment of affected camelids varied with the type and severity of clinical signs and laboratory abnormalities. The few with mild or no compatible clinical signs or laboratory abnormalities were mainly observed for evidence of worsening of their condition. Many camelids were transfused with 2 to 6 units (600 to 1,800 mL) of plasma in an attempt to maintain serum albumin concentration > 2 g/L and total plasma protein concentration > 4 g/L. One severely affected alpaca received 22 units (6.6 L) of llama plasma over an 18-day period. Other supportive treatments included IV administration of fluids to restore or maintain hydration; partial parenteral nutrition to decrease protein catabolism; antimicrobials to treat or prevent secondary bacterial infections; and flunixin meglumine for its antipyretic, anti-inflammatory, and antiendotoxic effects. Intravenous fluid administration was usually initiated after any initial plasma transfusions were given; fluid administration rate was no greater than 50 mL/kg/d (23 mL/lb/d) to avoid complications associated with overhydration in animals with hypoproteinemia. The constitution of the fluids varied with the abnormalities present each day for each case but generally consisted of a polyionic crystalloid solution with or without additives, such as potassium chloride or sodium bicarbonate, or consisted of a partial parenteral nutrition solution if fat mobilization or hepatic lipidosis was suspected.
Three camelids underwent surgical exploration because of persistent signs of colic and ultrasonographic findings of fluid-filled, atonic small intestine. No other cause for the clinical signs was identified. In only one of these patients was gross intestinal thickening (cobblestoning) identified. The llama with the gastric adenocarcinoma also underwent surgical exploration to investigate persistent weight loss and marked thickening of the wall of the third gastric compartment identified during ultrasonographic examination.
Specific treatment for E macusaniensis infection included oral administration of amprolium hydrochloride (10 mg/kg [4.5 mg/lb] in a 1.5% solution, PO, q 24 h for up to 15 days) or sulfadimethoxine (110 mg/kg [50 mg/lb], PO, q 24 h for up to 10 days). In a few cases, these agents were used in combination. Camelids treated with amprolium for > 5 days were also usually given thiamine hydrochloride (10 mg/kg, SC, q 24 h) after the fifth day. High dosages and extended periods of administration were used because of a perceived lack of efficacy in some of the first cases to be treated. In retrospect, these agents appear to have been most efficacious against earlier stages of the organism, and the increase in fecal oocyst counts and in the number of organisms found at necropsy in these first cases likely reflected maturation of later, more resistant stages of the organism. It is unknown whether treatment prior to admission of some camelids reduced overall shedding.
Seven of the 15 nonsurviving camelids died or were euthanized within 12 hours after admission to the Veterinary Teaching Hospital. The remainder, including 2 alpacas with hepatic lipidosis, 1 with colonic rupture, 1 with persistent azotemia, and the llama with carcinoma, survived between 2 and 8 days. For the 49 camelids as a group, mortality rate was 8/13 among individuals < 1 year old, 6/9 among individuals between 1 and 3 years old, 3/5 among individuals between 3 and 5 years old, and 12/17 among individuals ≥ 6 years old. We did not detect a significant association between age group and outcome (survived vs did not survive; χ2 test; P = 0.949).
The 15 surviving camelids generally were reported to progress well for at least 3 months after discharge. None was readmitted or reported to have further signs consistent with eimeriosis. Although infected camelids often lost weight prior to and during the hospitalization period, body weight often remained stable for up to 2 weeks after discharge before weight gain was noticed.
Discussion
Findings for camelids described in the present report suggest that E macusaniensis infection is a common cause of sickness and death among juvenile and adult camelids in the Pacific Northwest and can cause a spectrum of disease ranging from subclinical shedding to severe protein-losing enteropathy and death. Oocysts appeared to remain infective in the environment, with evidence suggesting they were capable of persisting in an ungrazed pasture for at least 6 months, which included a dry summer period.
Most previous reports concerning this parasite describe subclinical shedding,2–4,a but do not attribute sickness or death to infection by the organism, except in juveniles.5–8 As with most enteric coccidial infections, the prevalence of shedding among camelids without clinical signs of disease is highest among juveniles < 1 year old.6 Generally, other Eimeria spp are recovered more commonly and in higher numbers and are often found in conjunction with E macusaniensis.5,7,8 Eimeria macusaniensis is considered most pathogenic in conjunction with E lamae in juvenile camelids, but reports of it as a sole pathogen are rare. The possibility of fatal disease in an adult camelid has been mentioned previously,2 but such effects are generally underemphasized both in scientific reports and in the secondary literature on camelid health care.
Our findings suggest that adult camelids, particularly breeding-age females, comprise an important subset of infected camelids at this time. Immunity to coccidial organisms is thought to develop over time and to be suppressed by stress. In herds where infection is endemic, the adults in the herd tend to have developed immunity, leaving younger animals as the most susceptible to infection and disease. A previous report3 suggests that E macusaniensis is not widespread in Oregon. It is possible, therefore, that some of the adult camelids described in the present report, especially those with a history of recent transport, were exposed to novel Eimeria spp at the destination farm at a time when their immunity was reduced by the stress involved in transport, adjustment to a new environment, and establishment of social position within a new herd. Resident herdmates appeared to have been substantially more resistant.
Our findings suggest that the lack of importance previously attributed to E macusaniensis infection in adult camelids may relate to the prevalence of prepatent disease, difficulties in linking nonspecific or nonenteric disease signs to an enteric infection, an inability to isolate or recognize oocysts, the lack of gross lesions, or the segmental nature of histologic lesions. The evidence that E macusaniensis infection can be associated with a period of prepatent disease is strong. The life cycle for this parasite is considerably longer than the life cycles of other intestinal Eimeria spp that infect camelids, with reported prepatent periods of 32 to 36 days after first ingestion and 37 to 40 days after reinfection.a Seventeen of 42 (40%) camelids in the present report initially had negative fecal test results, even though many of these animals already had severe disease. Histologic examination of intestinal samples from 3 camelids revealed no stages more mature than the meront stage. The herd outbreak that was identified further supports the possibility of prepatent disease, in that 1 alpaca died as early as 20 days after presumed exposure and 17 days before herd members developed positive fecal test results. We suggest, therefore, that empirical treatment be considered in camelid patients with clinical abnormalities compatible with E macusaniensis infection, even if oocysts are not evident in the feces.
The most common disease signs reported for camelids included in the present report were nonspecific and not necessarily limited to signs of gastrointestinal tract disease. Only 18 of the 49 (37%) camelids had diarrhea and even fewer had colic or abdominal distention. Many of the other signs were referable to cachexia and protein loss, which may accompany many other diseases in camelids. Similarly, some signs were likely caused by secondary complications, including sepsis and hepatic lipidosis, or an unrelated disease, such as gastric carcinoma. Other signs, particularly those related to apparent dysphagia, were more difficult to connect to the illness but could possibly have been unusual manifestations of generalized weakness or have been related to laryngeal edema secondary to hypoproteinemia. Regardless, diagnosing illnesses in camelids has historically been a source of frustration for veterinarians. In instances when results of a fecal test are negative, this disorder has a high potential to be missed during a standard diagnostic evaluation. Analysis of serial fecal samples and examination of intestinal biopsy specimens or mucosal impression smears from camelids undergoing exploratory surgery because of colic or weight loss may aid in the diagnosis of E macusaniensis infection. In animals undergoing exploratory surgery, multiple intestinal samples should be submitted for histologic examination, even if the intestine appears grossly normal.
Clinicopathologic abnormalities in the camelids described in the present report were also generally nonspecific. Hypoproteinemia, hypoalbuminemia, hypokalemia, and hyperglycemia are reportedly common in sick camelids.9,10 Likewise, evidence of fat mobilization should be expected in camelids with anorexia. Hyponatremia is apparently uncommon in camelids and thus may potentially be suggestive of this or other enteric disorders. Severe hypoproteinemia without concurrent anemia or without anemia of corresponding severity also appeared to be a unique and relatively consistent finding in clinically affected camelids. In our clinical experience, sick camelids relatively commonly have total plasma protein concentrations < 4.0 g/dL and PCV < 25% with a variety of ailments, whereas hypoproteinemia without anemia is less common and may be suggestive of infection with E macusaniensis.
Only a few camelids in the present report developed gross intestinal abnormalities, even when heavily parasitized. Punctate mucosal plaques are reported to be common in camelids with undifferentiated coccidosis8 and with E macusaniensis and Eimeria ivitaensis coinfection.5 Proliferation of enteric mucosal elements resulting in grossly visible plaques or nodules is also a well-recognized lesion in sheep and goats with coccidiosis and has also been described in water buffalo with coccidiosis.11 Our findings suggest these plaques are rare in camelids with E macusaniensis infection.
The pathogenicity of coccidia is affected not only by the host response and ingested dose, but also by factors related to the life cycle of the infecting parasite. Many Eimeria spp, such as Eimeria bovis, cause considerable tissue damage by destroying the epithelial cells lining the gut, which results in exudation of host proteins and malabsorption. Other species of coccidia, such as Eimeria necratrix in chickens, cause most tissue damage as a consequence of rupture of schizonts in the lamina propria rather than as a result of parasite development in the epithelium.11 Eimeria macusaniensis is somewhat unusual in that many of the gamonts are located beneath the epithelial cell nuclei5 and may even be located with cells of the lamina propria. Ultrastructural studies would be required to make this distinction. Gamonts in the lamina propria have been described for other species of Eimeria, including Eimeria leuckarti in horses and Eimeria auburnensis in cattle. Eimeria macusaniensis is also reported to localize in the crypt regions of the intestine, where it can impair villus regeneration.5,8 A greater understanding of the life cycle of E macusaniensis may yield further clues as to the pathogenesis of this form of coccidiosis.
Flotation of E macusaniensis oocysts has been previously reported to be difficult.2 It is possible that infection may be missed when standard flotation techniques with saturated saline solution are used. It is also likely that infection may be missed in camelids with prepatent disease or when too few intestinal sections are examined histologically. Our findings and those of others5,8 suggest that severe lesions may be focal and concentrated in the distal portion of the jejunum or ileum and that remaining portions of the intestine frequently have few or no visible parasites. Harvesting multiple sections will enhance the likelihood of making a diagnosis.
The treatments used in the camelids described in the present report have not been evaluated in a controlled fashion but appeared to be associated with improvements in many camelids, including some with severe disease. Affected camelids commonly had evidence of circulatory shock, fat mobilization, and protein loss, and camelids that died also had evidence of shock, edema, bile stasis, renal insufficiency, hepatic lipidosis, muscle damage, relative hemoconcentration, and sepsis. Thus, treatment efforts should be directed at combating or preventing these pathologic processes in addition to killing the parasite. Efficacy of the anticoccidial medications that were used was difficult to determine because both amprolium and sulfadimethoxine are most efficacious against the early intestinal stages and thus may not immediately decrease or prevent fecal shedding.12 Evidence of this was seen in some of the camelids in the present report that had been treated prior to admission or during hospitalization and subsequently developed positive fecal test results or had an increase in oocyst count while undergoing treatment. It is still likely that treatment at the appropriate time with either of these agents would reduce survival of the multiplicative stages of the parasite and thus decrease intestinal damage.
In some of the infected camelids described in the present report, the infection was clearly severe enough to cause protein-losing enteropathy and many of the other clinical signs. In other camelids, only small numbers of parasites were seen on histologic or fecal examination and Eimeria infection may have been an incidental finding. However, it is important to remember the segmental or focal nature of some infections and the possibility of prepatent disease. Severity of disease ranged widely among camelids described in the present report, providing insight into the possible spectrum of clinical signs of disease. In small numbers, these parasites are unlikely to cause life-threatening or even clinical disease. It is likely that they act similarly to other enteric Eimeria spp in that light infections are benign, the organisms proliferate best in naïve hosts, and some degree of exposure is necessary to establish host immunity. Herds with ongoing exposure will likely develop group immunity so that disease will be uncommon among adults. However, given the severe disease present in many of the camelids in the present report, veterinarians should consider that the presence of even small numbers of oocysts could reflect a potentially fatal infection. Physical and laboratory assessments of infected camelids and, potentially, herdmates should be considered, especially if the camelids are showing clinical signs of disease or if this is the first time the parasite has been identified in the herd.
Rohbeck S, Gauly M, Bauer C. Biology of Eimeria macusaniensis in llamas (abstr), in Proceedings. 4th Eur Symp South Am Camelids, 2004.
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