History
Two adult male fox squirrels (Sciurus niger) from Kansas were observed with multiple areas of alopecia; 1 of the 2 animals was observed dragging its tail. The fox squirrels were euthanized by Kansas Department of Wildlife, Parks, and Tourism personnel and submitted to the Southeastern Cooperative Wildlife Disease Study in Athens, Georgia for diagnostic evaluation.
Gross Findings
Both fox squirrels (fox squirrels 1 and 2) had bilaterally symmetrical areas of alopecia in the axillary regions and along the dorsal midline (Figure 1). Multiple 0.5- to 1-mm-diameter pustules and a few small, superficial skin excoriations were present in the alopecic areas.
Photograph of 1 of 2 fox squirrels (Sciurus niger) from Kansas that were observed to be unwell and were euthanized. Notice the bilaterally symmetrical areas of alopecia in the axilla and along the dorsum. There are a few superficial excoriations along the dorsum and numerous pinpoint white pustules (arrows). Bar = 2 cm.
Citation: Journal of the American Veterinary Medical Association 253, 6; 10.2460/javma.253.6.723
Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page →
Histopathologic and Microbiological Findings
Sections of haired skin, brain, heart, liver, lungs, spleen, kidneys, pancreas, stomach, small intestine, large intestine, adrenal glands, and adipose tissue from each fox squirrel were examined histologically. The epidermis was diffusely, mildly to moderately hyperplastic with diffuse, basket-weave, orthokeratotic hyperkeratosis. There were scattered intraepithelial pustules, which occasionally contained cross sections through 100-μm-diameter arthropod parasites with a spined chitinous exoskeleton, hemocoel, segmented appendages, skeletal muscle, and gonads (Figures 2 and 3). Intraepithelial pustules were frequently associated with hair follicles that extended into the follicular space in the skin of fox squirrel 1. A few ruptured hair follicles were surrounded by abundant neutrophils, fibrin, and cellular debris (furunculosis) in the same squirrel. Adjacent epithelial cells were often compressed or separated by intercellular edema. The superficial dermis subjacent to epithelial pustules was often expanded by edema; in other areas, it was mildly fibrotic with atrophy or loss of adnexal structures and small numbers of perivascular lymphocytes and plasma cells. Deep skin scrapings of the alopecic skin of both fox squirrels revealed numerous approximately round, 150- to 200-μm-diameter, adult mites with 2 pairs of anterior and posterior limbs, long unbranched pedicels, and a dorsal anus, consistent with the genus Notoedres (Figure 4). Amplification and sequencing of the internal transcribed spacer-2 region of mite DNA revealed 99.4% similarity to a Notoedres centrifera sequence (GenBank accession No. KF278482) from a Western gray squirrel from California.1 The genetic sequences obtained from both fox squirrels were identical and were submitted to GenBank (accession No. KX344480).
Photomicrograph of a section of skin from fox squirrel 1. There is a focal intraepithelial pustule (arrows) containing a cross section through a mite (asterisk). The adjacent epithelium has mild to moderate acanthosis, spongiosis, and moderate orthokeratotic hyperkeratosis. The dermis subjacent to the pustule is mildly expanded by edema and infiltrated by small numbers of lymphocytes and plasma cells. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 253, 6; 10.2460/javma.253.6.723
Photomicrograph of another section of skin from fox squirrel 1. An intraepithelial pustule contains a cross-sectioned intrapustular mite. Notice the spined chitinous exoskeleton (arrow), jointed appendages (arrowheads), and hemocoel. These features are consistent with a sarcoptiform mite. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 253, 6; 10.2460/javma.253.6.723
Photomicrograph of a mite recovered from a deep skin scraping obtained from fox squirrel 1. This sarcoptiform mite has 2 pairs of anterior and posterior limbs and a dorsal anus (arrow), features that are consistent with the genus Notoedres. Bar = 50 μm. Inset—Long unbranched pedicels from the dorsal limbs of another mite recovered from a deep skin scraping obtained from fox squirrel 1.
Citation: Journal of the American Veterinary Medical Association 253, 6; 10.2460/javma.253.6.723
In the liver of fox squirrel 1, 2 discrete, round cysticerci (larval cestodes) surrounded by dense concentric rings of mature fibrous connective tissue had replaced and slightly compressed the adjacent hepatic cords. The 300-μm-diameter cysticerci were composed of a tegument surrounding a large bladder that contained an invaginated sco-lex and neck of the larval cestode with a parenchymatous body, calcareous corpuscles, and no gastrointestinal or reproductive tracts. There were no important histopathologic changes in sections of the brain, heart, lungs, spleen, kidneys, pancreas, stomach, small intestine, large intestine, adrenal glands, or adipose tissue of either fox squirrel or in sections of the liver of fox squirrel 2.
Morphologic Diagnosis and Case Summary
Morphologic diagnosis: moderate, chronic, locally extensive, hyperplastic dermatitis with orthokeratotic hyperkeratosis, multifocal intraepithelial pustules, and intrapustular mites.
Case summary: notoedric mange caused by N centrifera infestation in 2 fox squirrels.
Comments
Notoedres is a genus of sarcoptiform mites that have been detected in numerous mammalian hosts worldwide.2 Most of what is known about this genus is in regard to Notoedres cati, the causative agent of mange in domestic cats. Infestation with N cati in cats causes intense pruritus, leading to clinical signs that range from mild alopecia and crusting to self-trauma, severe secondary bacterial infections, and debilitation.3 The host range of N cati is not limited to cats, and infestation with this parasite in several mammalian species including humans has been reported.2,3 Humans in prolonged contact with infested cats can develop pruritic lesions most commonly on the hands, legs, and face, which spontaneously resolve after 1 to 2 weeks when affected persons are no longer exposed to infested cats.4 All life stages occur on the host and survival off the host is believed to be limited, although experimental trials with Sarcoptes scabiei suggest that mites may survive off hosts for several days in certain environmental conditions.5
Mites burrow through the epidermis and occasionally crawl to the skin surface during molting. Disease in the host is induced by the formation of burrows in the skin as well as immune reaction to secretions produced by the mites.2,6 Severity of disease varies among species and individuals, but clinical signs may include pruritus, alopecia, epidermal hyperplasia, and pustular dermatitis.6,7 Systemic signs including emaciation, dehydration, leukocytosis, lymphadenopathy, and secondary infection, and septicemia can also develop in cases of notoedric mange.6,8 Notoedric mange is highly contagious, and mites are transmitted between individuals by direct contact and potentially by recently contaminated fomites.2,9
Most frequently, notoedric mange in squirrels is caused by infestation with N centrifera.10 This species was first identified from black giant squirrels (Ratufa bicolor).11 In North America, Notoedres douglasi was considered the causative agent of notoedric mange in squirrels, but these 2 species were synonymized as N centrifera.12 This mite has been found on Western gray squirrels (Sciurus griseus), Eastern gray squirrels (Sciurus carolinensis), fox squirrels, Southern flying squirrels (Glaucomys volans), Eastern chipmunks (Tamias striatus), and porcupines (Erethizon dorsatum).9,13–16
Notoedres centrifera seems to be endemic in some wild squirrel populations in the United States, but there have been reports9,10,17 of periodic outbreaks of notoedric mange associated with large numbers of deaths among Western gray squirrels in California and Washington state, Eastern gray squirrels in Massachusetts, and fox squirrels in Indiana and Illinois. Most recently, N centrifera has been associated with a large die-off of Western gray squirrels in the San Bernardino mountains in California.16 The internal transcribed spacer-2 sequences derived from mites recovered from fox squirrels 1 and 2 in the present study most closely matched the sequences derived from mites associated with the outbreak in the San Bernardino mountains.
Sarcoptiform mange is the most commonly reported cause of alopecia in squirrels, but other differential diagnoses should be considered when alopecic skin lesions on squirrels are observed. Poxviruses, including squirrel fibroma virus in Eastern gray squirrels and squirrel parapox virus in American and European red squirrels, can cause alopecic, proliferative, crusting skin lesions similar to those that develop in cases of notoedric mange.18 Although unlikely in free-ranging animals, hair loss secondary to nutritional deficiencies in captive flying squirrels has been reported.19 Rare cases of diffuse idiopathic alopecia and epitheliotropic lymphoma in squirrels have also been reported.20,21
The history and gross and histologic findings for the affected animals described in the present report were similar to those reported previously for squirrels with notoedric mange.16 Affected squirrels are often euthanized because of severe disease, may die as a result of predation, or are found dead in nests or at the base of trees. On gross examination, the squirrels have thickened, alopecic, crusted skin around the ears, face, forelimbs, and trunk and often are in poor body condition.9,13,15–17 Characteristic histologic lesions include moderate to severe acanthosis with rete ridge formation, orthokeratotic or parakeratotic hyperkeratosis, intracorneal pustules, sections of intraepithelial tunnels containing numerous mites, and mild leukocytic infiltration of the underlying dermis.16 The severity of the lesions worsens with increasing mite burden.16 Ivermectin has been successfully used to treat notoedric mange in wild squirrels.7
Several risk factors have been suggested as potential promoters of notoedric mange outbreaks in wild squirrel populations. The development of clinical signs as a result of Notoedres infestation has been associated with stress and poor nutritional condition, potentially linked to crop failure during the previous season.9,13,14 Another possible predisposing factor for the development of notoedric mange is loss of natural habitat, which causes dispersal of squirrel populations and subsequently increases the opportunity for transmission of mites from affected to unaffected squirrels.9 Winter seasons with mild temperatures and high levels of precipitation may create environmental conditions that promote the survival of mites off the host and could increase the opportunity for transmission.10 Equipment used to trap, handle, and ear tag squirrels could also potentially act as fomites; therefore, appropriate care and actions should be taken to prevent iatrogenic transmission of the mites to potentially susceptible individuals.9
Both fox squirrels of the present report were in good nutritional condition, and there was no histologic evidence of underlying disease that may have predisposed them to ectoparasitism. The larval cestodes found in the liver of fox squirrel 1 were likely an incidental and unrelated finding. This is in contrast to companion animals, in which heavy mite burdens are uncommon and when present suggest an underlying immunocompromising condition that predisposes those animals to a more severe form of infestation (eg, so-called Norwegian scabies).6 There were no additional reports of affected squirrels from this geographic area, and the local population-level impacts were considered to be minimal, unlike the outbreak in Western gray squirrels.22
References
Zahler M, Essig A, Gothe R, et al. Molecular analysis suggests monospecificity of the genus Sarcoptes (Acari: Sarcoptidae). Int J Parasitol 1999;29:759–766.
Taylor MA, Coop RL, Wall RL. Veterinary entomology. In: Taylor MA, Coop RL, Wall RL, eds. Veterinary parasitology. 4th ed. Chichester, England: Wiley-Blackwell, 2015;221–222.
Foley RH. Parasitic mites of dogs and cats. Compend Contin Educ Pract Vet 1991;13:783–799.
Chakrabarti A. Human notoedric scabies from contact with cats infested with Notoedres cati. Int J Dermatol 1986;25:646–648.
Arlian LG, Vyszenski-Moher DL, Pole MJ. Survival of adults and development stages of Sarcoptes scabiei var. canis when off the host. Exp Appl Acarol 1989;6:181–187.
Gross TL, Ihrke PJ, Walder EJ, et al. Perivascular diseases of the dermis. In: Gross TL, Ihrke PJ, Walder EJ, et al, eds. Skin diseases of the dog and cat: clinical and histopathologic diagnosis. 2nd ed. Oxford, England: Blackwell Science Ltd, 2005;200–231.
Evans RH. Ivermectin treatment of notoedric mange in two fox squirrels. J Am Vet Med Assoc 1984;185:1437–1438.
Serieys LEK, Foley J, Owens S, et al. Serum chemistry, hematologic, and post-mortem findings in free-ranging bobcats (Lynx rufus) with notoedric mange. J Parasitol 2013;99:989–996.
Cornis TE, Linders MJ, Little SE, et al. Notoedric mange in Western gray squirrels from Washington. J Wildl Dis 2001;37:630–633.
Vander Haegen WM, Orth GR, Linders MJ. Survival and causes of mortality in a northern population of Western gray squirrels. J Wildl Manage 2013;77:1249–1257.
Jansen J. On the genus Notoedres Railliet, 1893, with a description of Notoedres centrifera n. sp. from the squirrel Ratufa bicolor. Ent Berichten 1963;23:258–264.
Fain S. Notes on the genus Notoedres Railliet, 1893 (Sarcoptidae: Sarcoptoformes). Acarologia 1965;7:321–342.
Carlson BL, Roher DP, Nielsen SW. Notoedric mange in gray squirrels (Sciurus carolinensis). J Wildl Dis 1982;18:347–348.
Lavoipierre MMJ. Mange mites of the genus Notoedres (Acari: Sarcoptidae) with descriptions of two new species and remarks on notoedric mange in the squirrel and the vole. J Med Entomol 1964;1:5–17.
Kazacos EA, Kazacos KR, Demaree HA. Notoedric mange in two fox squirrels. J Am Vet Med Assoc 1983;183:1281–1282.
Stephenson N, Swift P, Villepique JT, et al. Pathologic findings in Western gray squirrels (Sciurus griseus) from a notoedric mange epidemic in the San Bernardino Mountains, California. Int J Parasitol Parasites Wildl 2013;2:266–270.
Bryant HC. Tree squirrels infested with scabies. Calif Fish Game 1921;7:128.
Himsworth CG, Musil KM, Bryan L, et al. Poxvirus infection in an American red squirrel (Tamiasciurus hudsonicus) from Northwestern Canada. J Wildl Dis 2009;45:1143–1149.
Sheldon WG. Alopecia of captive flying squirrels. J Wildl Dis 1971;7:111–114.
Emmons RW, Maynard RP, Taylor DON. Total alopecia in a grey squirrel (Sciurus carolinensis). J Wildl Dis 1974;10:42–43.
Honnold SP, Arun I, Saturday G, et al. Epitheliotropic lymphoma in a squirrel (Sciurus sp.). J Zoo Wildl Med 2007;38:479–482.
Rudd J, Stephenson N, Clifford DL, et al. Utilizing citizen science to document a mange epidemic in Western gray squirrels in California. Wildl Soc Bull 2016;40:261–268.
