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Serum Chemistry, Hematologic, and Post-Mortem Findings in Free-Ranging

Bobcats (Lynx rufus) With Notoedric Mange

Article  in  Journal of Parasitology · August 2013

DOI: 10.1645/12-175.1 · Source: PubMed

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 Serum Chemistry, Hematologic, and Post-Mortem Findings in Free-Ranging
Bobcats (Lynx rufus) With Notoedric Mange
Author(s): Laurel E. K. Serieys , Janet Foley , Sean Owens , Leslie Woods , Erin E. Boydston , Lisa M.
Lyren , Robert H. Poppenga , Deana L. Clifford , Nicole Stephenson , Jaime Rudd , and Seth P. D. Riley
Source: Journal of Parasitology, 99(6):989-996. 2013.
Published By: American Society of Parasitologists
DOI: http://dx.doi.org/10.1645/12-175.1
URL: http://www.bioone.org/doi/full/10.1645/12-175.1

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 J. Parasitol., 99(6), 2013, pp. 989–996
Ó American Society of Parasitologists 2013

SERUM CHEMISTRY, HEMATOLOGIC, AND POST-MORTEM FINDINGS IN FREE-RANGING

BOBCATS (LYNX RUFUS) WITH NOTOEDRIC MANGE
Laurel E. K. Serieys, Janet Foley*, Sean Owens†, Leslie Woods†‡, Erin E. Boydston§, Lisa M. Lyrenjj, Robert H. Poppenga‡,
Deana L. Clifford#, Nicole Stephenson*, Jaime Rudd#, and Seth P. D. Riley}
Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095. Correspondence should be sent to: Laurelserieys@
gmail.com

ABSTRACT: Notoedric mange was responsible for a population decline of bobcats (Lynx rufus) in 2 Southern California counties
from 2002–2006 and is now reported to affect bobcats in Northern and Southern California. With this study we document clinical
laboratory and necropsy findings for bobcats with mange. Bobcats in this study included free-ranging bobcats with mange (n ¼ 34), a
control group of free-ranging bobcats without mange (n ¼ 11), and a captive control group of bobcats without mange (n ¼ 19). We used
2 control groups to evaluate potential anomalies due to capture stress or diet. Free-ranging healthy and mange-infected bobcats were
trapped or salvaged. Animals were tested by serum biochemistry, complete blood count, urine protein and creatinine, body weight,
necropsy, and assessment for anticoagulant rodenticide residues in liver tissue. Bobcats with severe mange were emaciated, dehydrated,
and anemic with low serum creatinine, hyperphosphatemia, hypoglycemia, hypernatremia, and hyperchloremia, and sometimes
septicemic when compared to control groups. Liver enzymes and leukocyte counts were elevated in free-ranging, recently captured
bobcats whether or not they were infested with mange, suggesting capture stress. Bobcats with mange had lower levels of serum
cholesterol, albumin, globulin, and total protein due to protein loss likely secondary to severe dermatopathy. Renal insufficiency was
unlikely in most cases, as urine protein:creatinine ratios were within normal limits. A primary gastrointestinal loss of protein or blood
was possible in a few cases, as evidenced by elevated blood urea nitrogen, anemia, intestinal parasitism, colitis, gastric hemorrhage, and
melena. The prevalence of exposure to anticoagulant rodenticides was 100% (n ¼ 15) in bobcats with mange. These findings paint a
picture of debilitating, multisystemic disease with infectious and toxic contributing factors that can progress to death in individuals and
potential decline in populations.

Until recently, notoedric mange caused by the mite Notoedres concurrently immunocompromised (Walton et al., 2004; Roberts
cati has only been reported in isolated cases in free-ranging felids et al., 2005). In Southern California a statistical association
(Penner and Parke, 1954; Pence et al., 1982; Maehr et al., 1995; between mange susceptibility in bobcats and anticoagulant
Pence et al., 1995; Ryser-Degiorgis et al., 2002). Severe mange and rodenticide (AR) exposure has been reported in which 39 bobcats
declining bobcat (Lynx rufus) populations were first observed in with advanced mange in SMMNRA tested positive for ARs in
2002 by the National Park Service (NPS) in Santa Monica liver samples (Riley et al., 2007); similar results have been found
Mountains National Recreation Area (SMMNRA), which in other California counties as well (Serieys et al., unpubl. data).
straddles Ventura and Los Angeles counties (Riley et al., 2007). Domestic cats are reported to be generally tolerant of low-grade
Coincident with the mange epizootic in 2002 in SMMNRA, there AR exposure (Erickson and Urban, 2004), although it is not
was a precipitous decline in the annual survival rate for radio- known whether this tolerance is experienced by other felids as
collared bobcats. Survival rates declined from a high of 0.847 in well. Sublethal toxicosis associated with chronic, low-grade
1999 (5-yr average, 0.770) to 0.280 by 2003 (Riley et al., 2007). exposure to ARs has been hypothesized to predispose bobcats
Since 2002, notoedric mange cases in bobcats have been to other medical conditions such as an inability to mount strong,
documented in at least 6 other Southern and Northern California anti-mite immunity (Riley et al., 2007). However, the physiologic
counties including Orange, San Diego, Santa Barbara, Santa mechanism by which AR exposure could potentially increase
Clara, Contra Costa, and Santa Cruz (Riley et al., 2007) bobcat susceptibility to notoedric mange is unknown. Other
(Boydston et al., unpubl. data; Serieys et al., unpubl. data). predisposing conditions that could exacerbate the susceptibility of
Severe mange in free-ranging and domestic animals is often
some free-ranging felid species to mange could include nutritional
associated with immunocompromise (Pence and Ueckermann,
and environmental stress, coinfection with other disease organ-
2002). Humans are more likely to suffer severe disease due to
isms, and genetic inbreeding or deleterious genetic conditions.
infestation with a related mite, Sarcoptes scabiei, if they are
Assessing the physiological parameters of bobcats with mange
could prove valuable to understanding the progression of disease
Received 30 December 2012; revised 22 July 2013; accepted 8 August
2013. in individual bobcats. In the present study, we report clinical
* Department of Medicine and Epidemiology, School of Veterinary serum biochemistry and complete blood count (CBC) values for
Medicine, University of California, Davis, California 95616. opportunistically sampled bobcats with severe mange in Southern
† Department of Pathology, Microbiology, and Immunology, School California. We compared serum biochemistry and CBC values of
of Veterinary Medicine, University of California, Davis, California bobcats with mange to data from a healthy control group of
95616.
‡ California Animal Health and Food Safety Laboratory System,
captive bobcats and free-ranging bobcats in Southern California
Davis, California 95616. with no evidence of mange and little evidence of chronic AR
§ U.S. Geological Survey, Western Ecological Research Center, 401 exposure. We evaluated the data for potential associations
West Hillcrest Road, Thousand Oaks, California 91360. between CBC and serum chemistry values and AR exposure.
|| U.S. Geological Survey, Western Ecological Research Center, 6010 We compare the percent body weight difference for 12 bobcats
Hidden Valley Road, Carlsbad, California 92011.
# California Department of Fish and Game, Wildlife Investigations
with healthy weights paired with mange-infested body weights.
Lab, 1701 Nimbus Road, Rancho Cordova, California 95670. We also present the results of necropsy examinations of 18
} National Park Service, Thousand Oaks, California 91360. bobcats with clinical mange. Finally, we compare urinalysis
DOI: 10.1645/12-175.1 results from a subset of free-ranging, apparently healthy bobcats

989
990 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 6, DECEMBER 2013

and mange-infested bobcats, presenting the first reported urine These body weights were compared with weights from the same bobcats
values for free-ranging captured bobcats. at a time when they were severely infested with mange.

Sample collection
MATERIALS AND METHODS
From captive, free-ranging healthy and from free-ranging, mange-
Bobcats infested bobcats 1 ml of blood was collected via venipuncture (n ¼ 45) or
Bobcats in this study included free-ranging bobcats with severe, cardiocentesis (n ¼ 1) into serum separating tubes and centrifuged within 1
clinical mange (n ¼ 16), a control group of free-ranging bobcats without hr of collection and the serum removed. One-half a milliliter of blood was
mange and minimal AR exposure (n ¼ 11), and a captive control group also collected into EDTA tubes. If available, urine was collected via
without mange (n ¼ 19). We used 2 control groups to evaluate potential cystocentesis of the urinary bladder. For 11 of 16 mange-infested bobcats
anomalies due to capture stress or diet. Prospective sampling occurred in that were moribund and died, 2 grams of liver were collected post-mortem
California in Los Angeles, Ventura, Orange, Contra Costa, and San and frozen at 20 C for AR analysis. Bobcat necropsies were performed
Diego counties during field studies conducted by National Park Service on fresh or previously frozen carcasses and were conducted by veterinary
(NPS) or United States Geological Survey (USGS) biologists. In Orange pathologists. For histopathology, tissues were fixed in 10% buffered
County, samples came from mange-infested bobcats that were found formalin, embedded in paraffin, thinly sectioned, and stained with
opportunistically during a USGS field study spanning 2005–2010. In Los hematoxylin and eosin.
Angeles and Ventura counties samples were collected from 2008–2011
during an ongoing bobcat ecology study begun in 1996 in SMMNRA. Notoedric mange evaluation
SMMNRA is 40 km from downtown Los Angeles and comprises 153,075 Skin scrapings were performed, at the time of capture for live animals
acres. SMMNRA encompasses large regions consisting of continuous or at the time of necropsy, on the head and just in front of the ears (sites
habitat with minimal urban development as well as fragmented areas reported to have the highest density of mites in infested animals) (Foley,
with low-to-high density residential development, golf courses, office 1991; Guaguère et al., 1999; Scott et al., 2001; Gross et al., 2005). Skin
buildings, and agricultural areas. Notoedric mange has been observed scrapings were performed as in Riley et al. (2007) and Stephenson et al.
throughout the park in bobcats except in the most continuous, natural- (2013). Briefly, tissue was scraped with a sterile surgical blade into mineral
core habitat in the western-most region of SMMNRA. oil and then examined microscopically under 3100 magnification. Mites
Bobcats with severe clinical mange were trapped or found in were identified as N. cati based on morphological criteria including length
SMMNRA (n ¼ 5) and Orange County (n ¼ 9), provided by a local and shape of stalks on anterior legs, lack of extension of posterior legs
resident in San Diego County (n ¼ 1), or provided by Animal Control in beyond the body, presence of body striations, and the dorsal position of
Contra Costa County (n ¼ 1). Three bobcats in SMMNRA were caught the anus (Lavoipierre, 1964; Klompen, 1992; Paterson, 2008). In 2 cases
in cage traps (Tru-catch traps, Belle Fourche, South Dakota) checked mites were reported as ‘‘consistent with Sarcoptes’’ although they were
every 12 hr as part of ongoing fieldwork. All other mange bobcats were more likely to have been Notoedres. Notoedric mange is the most common
found moribund and captured by residents using no capture devices or mite associated with feline mange (Malik et al., 2006) and sarcoptic and
captured by animal control officers using catchpoles. All bobcats with notoedric mites have few distinguishing characteristics. Further, previ-
mange, with the exception of the individual from San Diego County, ously published reports utilizing samples from Southern California have
were transported to a veterinary clinic for sampling. Individuals, with the detected only notoedric mites (Riley et al., 2007; Stephenson et al., 2013).
exception of the San Diego County case, were anesthetized with a
combination of approximately 6–10 mg/kg ketamine HCl and 0.05 mg/ Laboratory assays
kg medetomidine prior to sample collection. The San Diego County
individual died during transport to a clinic and was sampled within 5 min Serum chemistry and CBCs were performed at a commercial laboratory
of death via cardiocentesis. (IDEXX, Irvine, California; Antech Diagnostics, Irvine, California;
Captive bobcats were sampled at 2 rehabilitation facilities near the University of California Veterinary Medicine Teaching Hospital [VMTH],
study area in Ventura and San Diego counties. These bobcats had diets Davis, California). Urine evaluation was performed in the Chemistry
of rodents, poultry, beef, and commercial carnivore diet, and notoedric Laboratory of the VMTH. All pathogen testing reported here for
mange was not observed in any individuals in the collections. Individuals necropsied bobcats was done in laboratories at California Animal Health
in this group were anesthetized with approximately 5 mg/kg ketamine and Food Safety. Culture, serological, or molecular testing was ordered by
HCl and 0.1 mg/kg medetomidine by blow dart or jabstick, sampled, and the pathologist if gross or histopathologic lesions suggested particular
then returned to the collection. infectious causes.
Bobcats in the free-ranging control group (n ¼ 11) were sampled Residues of warfarin, coumachlor, bromadiolone, brodifacoum,
during ongoing fieldwork by NPS biologists in a protected state park diphacinone, chlorophacinone, and difethialone were assessed in bobcat
encompassing the most continuous and natural habitat in SMMNRA. livers by high performance liquid chromatography (HPLC) and LC-MS/
From 2008–2011, NPS biologists sampled bobcats in this region as part MS, as previously described (Riley et al., 2007; Ruder et al., 2011). Limits
of a radio-collaring study. Notoedric mange has not been reported for of quantitation for these anticoagulants vary according to their sensitivity
this population. Animals were captured in cage traps (Tru-catch traps, to UV or fluorescence detection during LC-MS/MS. In tissue these are
Belle Fourche, South Dakota) checked every 12 hr. Animals were 0.01 ppm for brodifacoum, 0.05 ppm for bromadiolone, warfarin, and
anesthetized with ketamine HCl 5 mg/kg and medetomidine 0.1 mg/kg coumachlor, and 0.25 ppm for chlorophacinone, diphacinone, and
and samples were collected in the field. Adult individuals in the free- difethialone. ARs that were determined to be positive by LC-MS/MS,
ranging healthy control group were radio-collared as part of the NPS but were below the limit of quantitation by HPLC, were defined as
study and had been documented to utilize only the western natural-core ‘‘positive.’’
region of SMMNRA. Individuals whose radio-collar locations were not
observed outside the boundaries of the protected state park areas during Data analyses
the course of the NPS study (Riley et al., unpubl. data) were used as free- Data analyses were performed using R statistical software (R
ranging controls because they were assumed to be at minimal risk for AR Development Core Team, 2010) and P-values of P  0.05 were considered
exposure. significant. For multiple statistical tests we used Bonferroni-corrected P-
An additional 18 free-ranging bobcat carcasses with mange from Los values. Summary statistics including the mean, standard deviation, and
Angeles, Ventura, San Diego, and Santa Barbara counties were available median were calculated for each group of bobcats for each chemistry and
for necropsy within 48 hr following death. One was euthanized shortly hematological parameter. All data were tested for normality using the
after being admitted to a wildlife rehabilitation center due to severe Shapiro-Wilk test for normality. Non-normally distributed values were
mange, 1 was hit by a car, 1 had trauma suggestive of predation, and all compared among bobcat groups using a Kruskal-Wallis test; normally
others had severe multisystemic disease and mange. distributed values were compared using ANOVA. For those blood
Body weights of 12 bobcats were obtained as part of the NPS long- chemistry parameters found to be statistically different using an ANOVA
term bobcat study in Los Angeles and Ventura counties when the or Kruskal-Wallis test, we performed either a Mann-Whitney or a Welch’s
individuals were in an apparently healthy state with no mange evident. t-test, respectively, for comparisons of each of the 3 groups. Within each
 SERIEYS ET AL.—CLINICAL FINDINGS OF MANGE-INFECTED BOBCATS 991

TABLE I. Mean, standard deviation (SD), and median for serum chemistry and hematological parameters for each bobcat group. *Indicates P  0.01
and † indicates P  0.001.

Mange Free-ranging healthy Captive ISIS‡

Parameter n Mean (SD) Median n Mean (SD) Median n Mean (SD) Median n Mean (SD)

Alkaline phosphatase (U/L) 15 11.9 (10.8) 8 11 16.3 (9.0) 15.5 19 35.1 (37.2) 13 130 19.0 (22.0)
Alanine aminotransferase (U/L)* 15 52.5 (54.0) 47 11 71.0 (35.1) 59 19 26.0 (6.0) 25 129 42.0 (20.0)
Aspartate aminotransferase (U/L)† 13 112.3 (95.1) 71 11 140.4 (81.8) 137.5 19 33.1 (10.5) 31 110 41.0 (22.0)
Albumin (g/dl)† 15 2.0 (0.8) 2 11 3.4 (0.3) 3.4 19 3.8 (0.2) 3.8 132 3.4 (0.7)
Total protein (g/dl)† 15 5.2 (1.9) 5 11 7.3 (0.3) 7.3 19 7.2 (0.5) 7.2 134 7.0 (0.7)
Globulin (g/dl) 15 3.2 (1.2) 3 9 3.9 (0.3) 3.9 19 3.4 (0.4) 3.4 132 3.7 (0.7)
Total bilirubin (mg/dl) 15 0.2 (0.1) 0.1 11 0.3 (0.1) 0.3 19 0.2 (0.1) 0.2 136 0.3 (0.2)
Blood urea nitrogen (mg/dl)† 16 84.0 (42.0) 89 11 39.0 (10.1) 40.5 19 35.1 (8.1) 38 143 32.0 (11.0)
Creatinine (mg/dl)† 14 0.7 (0.3) 0.7 11 2.0 (1.1) 1.5 19 1.8 (0.5) 1.8 140 2.0 (0.6)
Cholesterol (mg/dl)† 16 61.5 (43.1) 52 11 114.7 (42.4) 95 19 143.6 (30.0) 145 125 132.0 (36.0)
Glucose (mg/dl)† 15 82.0 (130.3) 42 11 212.4 (82.6) 211.5 19 167.8 (26.7) 167 132 171.0 (61.0)
Calcium (mg/dl)† 15 7.5 (1.8) 8 11 9.3 (0.5) 9.2 19 10.1 (0.5) 10.1 139 9.8 (0.7)
Phosphorus (mg/dl)† 15 8.0 (3.2) 7.3 11 5.0 (1.1) 4.9 19 5.1 (1.5) 4.5 128 5.4 (1.4)
Chloride (mmol/L)† 16 129.9 (10.0) 134 11 120.1 (4.8) 120.2 19 119.5 (2.0) 120 140 120.0 (5.0)
Potassium (mmol/L) 16 4.3 (1.3) 4 11 4.2 (0.4) 4.1 19 4.1 (0.4) 4.1 137 4.5 (0.6)
Sodium (mmol/L) 16 156.0 (14.3) 159 11 153.1 (4.8) 153 19 152.5 (1.3) 153 137 152.0 (4.0)
Leukocytes (K/ll)* 9 19.3 (12.9) 22.9 11 13.9 (4.0) 15.5 10 7.3 (2.7) 6.3 135 6.9 (5.1)
Neutrophils (K/ll)* 9 15.4 (11.0) 17.6 11 11.6 (4.3) 11.6 10 4.8 (2.6) 3.8 123 4.2 (3.9)
Lymphocytes (K/ll) 9 1.4 (0.8) 1.4 11 1.5 (0.8) 1.2 10 1.8 (0.5) 1.7 129 2.1 (1.8)
Monocytes (K/ll)* 9 0.7 (0.4) 0.7 11 0.4 (0.2) 0.3 10 0.2 (0.1) 0.2 113 0.2 (0.3)
Eosinophils (K/ll)* 9 1.7 (1.6) 1.9 11 0.4 (0.2) 0.3 10 0.4 (0.2) 0.4 117 0.5 (0.4)
Basophils (K/ll) 9 0.0 (0.1) 0 11 0.0 (0.0) 0 10 0.0 (0.0) 0 23 0.3 (0.7)
Hematocrit (%)† 9 23.8 (11.2) 18.7 11 40.4 (3.7) 40.6 10 34.3 (7.2) 36.3 148 36.7 (6.1)
Platelets (K/ll) 9 485.3 (144.7) 503 11 402.8 (74.0) 404 10 384.0 (138.0) 409 73 407.0 (143.0)

‡ 2011, International Species Information System (ISIS), Apple Valley, Minnesota 55124-8151, USA.

group we also tested for differences between males and females for each total bilirubin, and potassium, mean or median values did not
blood parameter using a Mann-Whitney or a Welch’s t-test. Differences differ from VMTH-established normal reference intervals for
between healthy and clinically mange-infested bobcats’ urine protein and
creatinine levels were assessed with 2-tailed Student’s t-tests as were
domestic cats or International Species Information System (ISIS)
differences in body weights for bobcats while healthy and while infested values for bobcats (Flesness, 2003). Correlations were not
with mange. Differences between anticoagulant concentrations in necrop- observed between blood chemistry parameters and anticoagulant
sied bobcats with evidence of gastrointestinal hemorrhage, compared with residue concentrations.
those without hemorrhage, were performed using a Mann-Whitney test.
Although alanine aminotransferase (ALT) values tended to be
Finally, for animals for which we had anticoagulant residue results paired
with hematological parameters, we tested for correlations between AR within the normal reference interval for all 3 bobcat groups, the
concentrations and blood chemistry and hematocrit values using Spear- healthy captive bobcats had significantly (P  0.01) lower mean
man’s test. ALT levels compared with both the mange-infested and free-
ranging healthy bobcats (Table I). Captive bobcats did not have
RESULTS elevations in aspartate aminotransferase (AST) while both
healthy and mange-infested free-ranging bobcats had significantly
Of the 15 animals examined at a veterinary hospital, 10 were in
(P  0.001) elevated values that were more pronounced in the
moribund condition and 11 died within 24 hr of sample collection
free-ranging healthy bobcats. Serum albumin, total protein,
despite treatment that included administration of fluids, vitamin
creatinine, cholesterol, and calcium were significantly (P 
B, antibiotics, and acaricides. In each case, a veterinarian or
0.001) decreased in bobcats with mange compared to both free-
veterinary pathologist attributed the cause of mortality to mange-
ranging healthy and captive healthy bobcats, and the values for
related complications.
these infested bobcats were lower than the normal reference
interval. All 3 bobcat groups had mean BUN levels that exceeded
Clinical serum chemistry
reference intervals, and this was significantly (P  0.001) elevated
Serum chemistry values for captive healthy, free-ranging in mange-infested bobcats. Glucose values were particularly
healthy, and free-ranging mange-infested bobcats were compared difficult to characterize: both free-ranging and captive healthy
by group (Table I). Serum total protein, blood urea nitrogen bobcats tended to have values above the normal reference interval
(BUN), phosphorus, and chloride were normally distributed and while mange-infested bobcats had a mean glucose of 82 mg/dl,
thus compared by ANOVA; the other analytes had non-normal which was significantly (P  0.001) lower than that for the
distributions for at least 1 bobcat group and so were analyzed by healthy bobcat groups. Serum phosphorus and sodium were
Kruskal-Wallis test. For serum alkaline phosphatase, globulin, within normal limits in both captive and free-ranging healthy
992 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 6, DECEMBER 2013

bobcats but were significantly (P  0.001) elevated in bobcats Affected skin was alopecic with adherent crusts, excoriations, and
with mange. lichenification in chronic cases. Microscopically, the dermatitis
was characterized by acanthosis, hyperkeratosis, and parakera-
Complete blood counts tosis with serocellular crusts and subcorneal pustules; mites were
numerous and embedded in the epidermis. Two individuals had a
Complete blood counts were performed on samples from 30 of
concurrent Malassezia dermatitis. In 4 bobcats gastrointestinal
46 bobcats in the same free-ranging mange-infested, free-ranging
contents resembled hemorrhage. Other findings in bobcats
healthy, and captive healthy control groups (Table I). Statistically
included splenic or lymph node lymphoid depletion, histiocytosis,
significant differences among groups were detected in hematocrits
or both, bacteremia due to Staphylococcus xylosus, Escherichia
and in leukocyte, neutrophil, monocyte, and eosinophil counts.
coli, or coagulase-negative Staphylococcus sp., degenerative
Mange-infested bobcats had a leukocytosis with a mean leukocyte
changes in the adrenal gland, chronic leptospirosis associated
count of 19,300/ll (range 2,800–39,600/ll) compared with 13,900/
with Leptospira pomona, pneumonia, respiratory nematodes, or
ll (2,800–20,100/ll) in free-ranging healthy and 7,300/ll (4,000–
enterocolitis (Table II). Three bobcats were tested for Toxoplasma
11,7000/ll) in captive healthy bobcats. Similarly neutrophil,
gondii antibodies by latex agglutination and 2 were positive. Of 6
monocyte, and eosinophil counts were elevated in mange-infested
that were tested for FeLV and FIV by ELISA, all were negative
bobcats compared with free-ranging healthy and captive healthy
(Table III). Six bobcats were also tested for rabies virus by
bobcats. Although the trend for these white blood cell counts was
fluorescent antibody testing and all were negative.
higher in mange-infested bobcats, their values ranged widely
(neutrophils 700–31,000/ll, monocytes 200–1,200/ll, eosinophils Anticoagulant residue analysis
50–4,300/ll) compared with free-ranging healthy (neutrophils
3,420–18,090/ll, monocytes 161–820/ll, eosinophils 160–640/ll) Liver samples from 27 mange-infested bobcats were tested for
and captive control bobcats (neutrophils 2,000–9,360/ll, mono- AR exposure (Table IV) and all 27 were exposed to anticoagu-
cytes 80–585/ll, eosinophils 126–918/ll). Significant differences lants. Four different ARs were detected in bobcats: brodifacoum,
between groups after correction for multiple tests were observed bromadiolone, diphacinone, and difethialone, and 21 of the 27
between the captive healthy and mange-infested groups for exposed bobcats had residues of 2 or more compounds. Bobcats
monocytes and eosinophils (P ¼ 0.003 for each test). Free-ranging with AR exposure were from Orange, San Diego, Los Angeles,
healthy bobcats also had significantly higher leukocytes (P , Ventura, Santa Clara, San Diego, and Santa Barbara counties.
0.001), neutrophils (P , 0.001), and monocytes (P ¼ 0.01) Anticoagulant residue concentrations were not observed to
compared with captive healthy bobcats. Hematocrits in mange- correlate with gastrointestinal hemorrhage for necropsied indi-
infested bobcats ranged from 10.9–40.0%, with a mean of 23.8%, viduals, although our sample size was small. Two bobcats without
compared with means of 40.4% (range 36.4–42.9%) in free- mange from the free-ranging healthy control group used for this
ranging healthy and 34.3% (range 24.0–45.0%) in captive healthy study were also positive for AR in liver tissue, both at levels below
bobcats. Hematocrits did not correlate with AR residue the minimum level for quantification. These were the only liver
concentrations. samples available for testing from the free-ranging healthy bobcat
group. However, clotting times measured by partial thrombo-
Urine values plastin time and proteins invoked in Vitamin K absence for all
free-ranging healthy bobcats were within normal limits at the time
Urine specific gravities ranged from 1.027 to .1.040, confirm- of their capture and blood collection for use in this study (Riley et
ing renal sufficiency. Urine protein:creatinine ratios were assessed al., unpubl. data; Serieys et al., unpubl. data).
in 9 bobcats in order to determine whether renal protein loss was
occurring. Four of these samples came from bobcats with mange, Body weight
and the mean and standard deviations were 45.0 mg/dl (615.9)
for protein values and 312.4 (6277.3) for creatinine. Protein Paired healthy and mange-infested body weights were available
values in the 5 healthy bobcats were 84.4 (6125.6) and creatinine for 11 adult bobcats (4 male, 7 female) and 1 juvenile male.
values were 207.8 (6125.6). These differences were not statisti- Weight loss was attributed to severe mange-infestation and the
cally significant. Only 1 protein:creatinine ratio, in a clinically mean body weight difference across males and females was 39%.
healthy bobcat, exceeded 1 and that urine sample was frankly The mean weight loss was the same for both males and females
blood-contaminated. and ranged from 30–56% (P ¼ 0.002 for males and P , 0.001 for
females).
Necropsy
DISCUSSION
Necropsies were performed on 18 bobcats from 4 counties in
California. Eleven of these bobcats were male, 6 were female, and Notoedric mange is a potentially fatal and emerging disease of
for 1 bobcat the sex was not recorded. There were 11 adults, 5 concern in bobcat populations in California. Ongoing ecological
juveniles, and 4 for which the age group was not recorded. All studies suggest that mange may contribute to bobcat population
bobcats that were necropsied ranged from thin to emaciated and regulation and decline. However, mange per se often is not
all had moderate to severe mange confirmed by microscopic considered fatal, and thus we sought to understand what medical
examination of skin scraping. In addition, bobcats were infested factors might underlie and then contribute to the progression of
with various endoparasites and ectoparasites as shown in Table such severe disease. In this study, the majority of bobcats with
II. All bobcats had a severe dermatitis which consistently affected mange were emaciated and dehydrated, had severe panhypopro-
the head, ears, and neck and, in severe cases, was generalized. teinemia, probably due to a protein-losing dermatopathy, and
TABLE II. Summary of necropsy data from 18 bobcats with notoedric mange. *Indicates histopathology performed. C: cestodes. A: ascarids. N: nematodes. WNL: within normal limits. LN:
lymph nodes. N/A: not examined.

ID Endoparasites Ectoparasites Gastrointestinal Lymphopoetic Hepatic Urogenital Pulmonary Other

D22* C, A M colitis WNL hemosiderosis WNL WNL degenerative myopathy

D03* C M, T WNL LN erythrophagocytosis WNL interstitial nephritis pneumonia none
D45* C M WNL lymphoid depletion hepatocellular renal tubular WNL keratitis
vacuolation vacuolation
D27* C, A M WNL lymphoid depletion WNL interstitial nephritis WNL none
S40 A M WNL WNL hepatocellular WNL N/A none
degeneration
and necrosis
D16* A M melena grossly enlarged LNs WNL WNL WNL none
D66* N/A M WNL reactive LN with WNL WNL Interstitial pneumonia Presumptive
erythrophagocytosis hypoproteinemia,
serous atrophy of fat,
myocytic protozoa,
thyroid follicular
collapse
B66* C M unidentified lymphadenopathy congestion, glomerulosclerosis WNL none
intraenterocyte hemosiderosis,
structures lipidosis
D36* C, A M, T, F WNL WNL WNL WNL pulmonary edema Salmonella D1, fat
atrophy, yeast
D13* C M WNL prescap LN enlarged WNL interstitial nephritis, WNL hemorrhage,
lymphocytic meningoencephalitis,
yeast
D96* C, A M WNL lymphoid depletion enlarged WNL hemorrhage (iatrogenic) euthanized
D42* A M, T WNL lymphoid depletion WNL, WNL E. coli pneumonia severe thyroid atrophy
lymphofollicular Escherichia
hyperplasia, coli isolated
lymphadenopathy
B71* N M WNL lymphadenopathy WNL pale with WNL trauma–HBC
lymphoplasmacytic
infiltrates
B18* C, A M, F gastric N/A N/A renal foci of unknown white nodules on lung none
hemorrhage cause, chronic
multifocal
B72 N M, F WNL white pulp depletion WNL WNL WNL ocular N
B60 N T enterocolonic WNL WNL adhesion N none
hemorrhage
B68 N, C M small intestinal LNs blackened WNL WNL WNL none
hemorrhage
B19 N, C T hemorrhagic WNL nematode WNL WNL trauma–predation
gastritis, colitis migration
SERIEYS ET AL.—CLINICAL FINDINGS OF MANGE-INFECTED BOBCATS
993
994 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 6, DECEMBER 2013

TABLE III. Results of diagnostic tests performed on bobcats as part of necropsy examination. Y: yes. Pos: positive. Neg: negative. —: test not
performed.

ID AR Toxoplasmosis Leptospirosis Felv–FIV Rabies FIP

D22 Y pos neg neg — —

D03 Y — pos neg — —
D45 Y neg neg neg — neg
D27 Y — pos neg — —
S40 — — — — — —
D16 Y — — — — —
D66 — — — — — —
B66 Y pos — neg neg —
D36 Y — — — — —
D13 Y — — — neg —
D96 Y — — — neg —
D42 Y — — — — —
B71 Y — — neg — —
B18 Y — — — — —
B72 — — — — — —
B60 Y — — — — —
B68 Y — — — — —
B19 Y — — — — —

were exposed to ARs. Overall these findings paint a picture of a larly leukocyte counts (Kocan et al., 1985; Marco and Lavin,
severe multisystemic disease that may result from infectious and 1999). However, in mange-infested bobcats several liver function
toxic injury but leads to death in individuals and a decline in indicators were abnormal including albumin, glucose, and
populations. cholesterol. Although necropsy did not indicate widespread liver
CBC and serum chemistry findings can be important sources of pathology in mange-infested bobcats, we believe that emaciation,
information in ecological studies of bobcats and can serve as protein loss, bleeding, or sepsis (or any combination) can account
indicators of nutritional status, disease, trauma, habitat quality, for these abnormal values.
and other environmental stressors (Fuller et al., 1985; Kocan et Bobcats with mange had low levels of cholesterol, albumin
al., 1985; Heidt et al., 1988; Knick et al., 1993). By compiling (which accounts for the low serum calcium), globulin, and total
chemistry, hematological, necropsy, and AR exposure results, we protein. Given the lack of significant liver pathology, it is likely
identified particular systems that appear to be targeted during the that protein production was normal and there was no evidence of
development of severe mange. There were multiple indicators renal protein loss. Rather, the protein loss is most likely
consistent with chronic disease, emaciation, and dehydration: secondary to severe dermatopathy. In fact, the severity of the
these include anemia (due to blood loss or chronic disease), low dermatopathy was similar to crusted scabies in people, an extreme
creatinine (emaciation), and hyperphosphatemia (dehydration). form of mange characterized by large numbers of mites, high IgG
The leukocytosis observed in many of the bobcats with mange is and IgE levels, and the development of hyperkeratotic skin crusts
consistent with, although not diagnostic for, an inflammatory over extensive regions of the body (Walton et al., 2004). In these
process. Similar to our findings, eosinophilia was observed in cases, skin lesions often become secondarily infected and regional
humans infested with sarcoptic mange (Falk and Matre, 1982) lymphadenopathy is common. Interestingly, three of the bobcats
while neutrophilia was observed in laboratory rabbits infected had adrenal enlargement, which can occur secondary to chronic
with sarcoptic mange (Arlian et al., 1988). The abnormal stress or immune stimulation and also produce immunosuppres-
leukocyte counts observed in bobcats with mange suggest sive glucocorticoids which could exacerbate mange.
pathological conditions resulting from severe infestation. While the protein loss in the skin of these bobcats was
Liver enzymes ALT and AST, neutrophils, and monocytes were considerable, it is also important to determine whether there were
elevated in free-ranging, recently captured bobcats whether or not other sources of protein loss; however, there was no evidence of
they were infested with mange, suggesting that these elevations third space protein loss on necropsy. Renal disease was not
are due to capture stress. Previous research has indicated that supported on necropsy except for a few cases such as those of
capture stress can influence hematological parameters, particu- leptospirosis. Moreover, there was no evidence for protein-losing
nephropathy based on urine protein:creatinine ratios. Some of the
TABLE IV. Summary of results of anticoagulant rodenticide testing in bobcats did have evidence of pre-renal azotemia secondary to
livers of bobcats with notoedric mange. dehydration (azotemia, hyperchloremia, hypernatremia, high
urine specific gravity, and hyperphosphatemia).
Anticoagulant Brodifacoum Bromadiolone Diphacinone We are concerned about a primary gastrointestinal loss of
protein or blood in some of the bobcats. Gastrointestinal bleeding
Number of positive bobcats 19 19 5
is consistent with the observed anemia and increased BUN in the
Maximum residue level (ppm) 0.68 1.4 0.75
Mean residue level (ppm) 0.23 0.62 0.49
absence of increased serum creatinine, but the elevated BUN
could also be due to a high protein diet or emaciation. We could
 SERIEYS ET AL.—CLINICAL FINDINGS OF MANGE-INFECTED BOBCATS 995

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