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Faccin Et Al 2023 Common Superficial and Deep Cutaneous Bacterial Infections in Domestic Animals A Review

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Faccin Et Al 2023 Common Superficial and Deep Cutaneous Bacterial Infections in Domestic Animals A Review

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© © All Rights Reserved
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1176558

review-article2023
VETXXX10.1177/03009858231176558Veterinary PathologyFaccin et al

Review
Veterinary Pathology

Common superficial and deep cutaneous 2023, Vol. 60(6) 796­–811


© The Author(s) 2023
Article reuse guidelines:
bacterial infections in domestic animals: sagepub.com/journals-permissions
DOI: 10.1177/03009858231176558
https://doi.org/10.1177/03009858231176558

A review journals.sagepub.com/home/vet

Mayane Faccin1, Dominique J. Wiener1, Raquel R. Rech1, Domenico Santoro2,


and Aline Rodrigues Hoffmann2

Abstract
The skin covers the external surface of animals, and it is constantly exposed to and inhabited by different microorganisms,
including bacteria. Alterations in the skin barrier allow commensal and/or pathogenic bacteria to proliferate and penetrate
deep into the lower layers of the skin. Being the first barrier to the external environment, the skin is prone to injuries, allowing
the penetration of microorganisms that may lead to severe deep infections. Companion animals, especially dogs, are prone
to bacterial infections, often secondary to allergic dermatitis. When environmental conditions are unfavorable, horses, cattle,
sheep, and goats can develop superficial infections, such as those caused by Dermatophilus congolensis. Deep inflammation is
commonly caused by Mycobacterium spp., which results in granulomatous to pyogranulomatous dermatitis and panniculitis.
Likewise, bacteria such as Nocardia spp. and Actinomyces spp. can cause deep pyogranulomatous inflammation. Bacteria that lead
to deep necrotizing lesions (eg, necrotizing fasciitis/flesh-eating bacteria) can be severe and even result in death. This review
includes an overview of the most common cutaneous bacterial infections of domestic animals, highlighting the main features and
histologic morphology of the bacteria, cutaneous structures involved, and the type of inflammatory infiltrates.

Keywords
bacteria, dermatitis, folliculitis, furunculosis, panniculitis, pyoderma, review, skin, vasculitis

The skin is the largest organ in the body and provides an external The Microbiome Inhabiting the Skin
barrier to the organism. It is also constantly exposed to and inhab- Surface of Domestic Animals
ited by different microorganisms, including bacteria. Alterations
in the skin barrier allow commensal and/or pathogenic bacteria to It is well established that the skin harbors a variety of microor-
proliferate and penetrate deep into the lower layers of the skin. ganisms, including viruses, bacteria, archaea, and fungi, as
Different superficial and deep bacterial infections will lead to well as mites.17,36 Compared to humans, animals have a higher
different lesion patterns involving the skin of animals (Fig. 1a– diversity of their microbiota. The microbiota is primarily influ-
d). For instance, the overgrowth of pathogenic bacteria coloniz- enced by the host taxonomic order and geographical location,81
ing the skin surface is more likely to result in superficial pustules. with the canine microbiota being mainly influenced by indi-
However, with skin barrier disruption, bacteria can penetrate the vidual variability and body site.79 The most common bacterial
skin and result in deep suppurative to pyogranulomatous phyla found on dog skin are Proteobacteria, Actinobacteria,
inflammation. Certain bacteria, such as Mycolicibacterium spp. Firmicutes, Bacteroidetes, and Fusobacteria.80 Cats are inhab-
(former Mycobacterium spp.), are attracted by lipid-rich envi- ited by similar bacterial phyla, although Bacteroidetes is one
ronments53 and will often cause panniculitis. It is crucial for of the most prevalent phyla on their skin.65 This phylum
pathologists to identify the distribution and pattern of lesions predominates in their oral cavity, and it is suggested that the
involving the skin to narrow down possible differential diagno-
ses of cutaneous infections. This review focuses on the most 1
Texas A&M University, College Station, TX
common cutaneous bacterial diseases of domestic animals, high- 2
University of Florida, Gainesville, FL
lighting the characteristic clinical and histologic lesions. It is
Supplemental material for this article is available online.
divided into five sections, discussing the normal cutaneous
microbiota inhabiting the skin of domestic animals and the Corresponding Author:
Aline Rodrigues Hoffmann, Department of Comparative, Diagnostic, and
pathogens associated with cutaneous infections based on the
Population Medicine, College of Veterinary Medicine, University of Florida,
affected portion of the skin, such as epidermis, hair follicles, der- PO Box 1001123, 2015 SW 16th Ave., Gainesville, FL 32610, USA.
mis and panniculus, and blood vessels. Email: [email protected]
Faccin et al 797

Figure 1. Schematic representation of the main patterns of bacterial diseases affecting the skin and the differential diagnoses associated
with each pattern. (a) Bacterial diseases that affect the epidermis. These are often characterized by pustules that may extend to the
follicular ostia filled with degenerate neutrophils and occasional acantholytic cells. Chronic lesions can also result in crusts with cellular
debris, epidermal hyperplasia, and hyperkeratosis. Bacteria may be present within the pustules, crusts, or in the hair follicle opening. (b)
Bacterial diseases that affect the hair follicles. This type of infection causes folliculitis with rupture of the hair follicles, leading to furunculosis
and the formation of draining tracts with ulceration of the overlying epidermis. In some conditions, such as postgrooming furunculosis and
German Shepherd pyoderma, hemorrhagic bullae can be present. In chronic cases, apocrine adenitis can also be observed. (c) Bacterial
diseases affecting the dermis and panniculus. This group of diseases results in nodular inflammation involving the dermis and panniculus.
It can lead to draining tract formation, as well as ulceration of the overlying epidermis. This type of inflammatory response will vary from
suppurative to granulomatous or pyogranulomatous. The presence of organisms within the lesions varies, and special stains are often
required. (d) Bacterial diseases affecting the blood vessels. This group results in vasculitis characterized by fibrinoid necrosis, thrombosis,
and hemorrhage. Both superficial and deep blood vessels may be affected. The causative agent is usually not seen in the histological sections.

cats’ grooming behavior is responsible for spreading the bacte- competitors. Commensal species, including Cutibacterium
ria to other body sites.65 The most common bacterial genera on acnes (formerly Propionibacterium acnes) and Staphylococcus
equine skin include Psychrobacter, Macrococcus, Pseudomonas, epidermidis, can metabolize lipids,18 leading to the production
Acinetobacter, Planomicrobium, Arthrobacter, Carnobacterium, of antimicrobial metabolites and decreased cutaneous pH,
Desemzia, and Corynebacterium, and the microbiota composi- which creates a hostile environment for pathogenic organ-
tion in this species is mainly influenced by body site.70 In cattle, isms.36 Another survival strategy is the microbial production of
microbiome studies have focused on the udder, which is pre- bacteriocins and antimicrobial peptides (AMPs). Several coag-
dominantly colonized by the families Corynebacteriaceae and ulase-negative staphylococci, such as S. epidermidis, S. homi-
Staphylococcaceae,76 and the feet.101 nis, and S. felis have been shown to produce AMPs that inhibit
The skin is a nutrient-poor environment, which by itself the growth of Staphylococcus aureus and S. pseudinterme-
regulates the composition of its bacterial community. Among dius.19,20,43,60,68 S epidermidis can also induce the production of
the bacteria that can successfully survive and colonize the skin, AMPs by the host (also known as host defense peptides), which
some have developed additional strategies to thrive over their can synergistically promote and modulate the immune response,
798 Veterinary Pathology 60(6)

increasing the effectiveness of the innate immune populations of Staphylococcaceae in their skin compared to
response.19,20,31,60,82,90 healthy dogs, especially in the groin and nostrils.12,79 The main
Cutaneous dysbiosis is defined as an imbalance of skin bac- conditions associated with pyoderma are hypersensitivities,
terial populations.31 Two models of dysbiosis have been pro- atopic syndromes, ectoparasites, endocrinopathies, dermato-
posed to explain why this phenomenon occurs: (1) dysbiosis phytosis, and cornification abnormalities.10,49,87 A recent study
driven by microbial communities, where a shift in microbial has shown that 68% of the dogs diagnosed with recurrent pyo-
composition alters the immune response, leading to damage to derma had one of the aforementioned underlying conditions
the barrier homeostasis and subsequent penetration or over- with allergies being the most common (59%).87 Other reasons
growth of harmful bacteria; (2) dysbiosis driven by host biol- why dogs are considerably more predisposed to pyoderma are
ogy/pathology that alters the barrier and/or immune system and related to specific characteristics of the canine stratum cor-
changes the composition and distribution of the microbial pop- neum, which is thinner and more compact than in other species,
ulation, which results in bacterial overgrowth or penetration lacks a lipid follicular plug, has decreased intercellular lipids,
and leads to impaired or inappropriate immune responses.31 and has a higher pH.33 These characteristics may favor the sur-
Regardless of the mechanism, dysbiotic conditions alter the vival and adherence of staphylococci on canine skin.
cutaneous bacterial populations, which can lead to disease. Dogs present with papules, pustules, and epidermal collar-
ettes with peripheral erythema and exfoliation, particularly
involving the abdomen, groins, and axillae (Fig. 2a, Supplemental
Bacterial Diseases Affecting the
Fig. S1b–d).33,49 Alopecia is variable.38 Cytological evaluation at
Epidermis the margins of the epidermal collarettes is recommended, where
Pyoderma can be classified into three categories based on the bacteria and neutrophils are far more easily detectable, compared
depth of the inflammation/infection: surface pyoderma, super- to the center of the collarette.5 Histologically, pustules with neu-
ficial pyoderma/folliculitis, and deep pyoderma and furunculo- trophils and a variable number of eosinophils are in the superfi-
sis.10 Surface pyoderma is the least understood category of cial epidermis, and infundibulum or ostium of superficial hair
pyoderma and comprises pyotraumatic dermatitis and fold der- follicles (Fig. 2b), with or without few acantholytic keratino-
matitis (intertrigo, Supplemental Fig. S1a). In surface pyo- cytes. Bacteria are not always detected, and crusts are common
derma, bacteria are confined to the skin surface with a dominant with older pustules. Inflammation can also follow the isthmus
inflammatory response.49 Some authors also include bacterial and encircle adnexal glands. In some cases, the inflammatory
overgrowth syndrome in this category,49 although this may not infiltrate can pierce the hair follicle infundibulum, leading to
be considered a true pyoderma, as it lacks neutrophilic superficial perforating folliculitis. This phenomenon is distinct
inflammation.33 from furunculosis, as it remains superficial and does not efface
Superficial pyoderma primarily involves the epidermis and the entire follicle.38
can extend into the upper portion of the hair follicles. In deep
pyoderma, rupture of hair follicles leads to the expansion of the
Impetigo
inflammation toward the adjacent dermis and deep into the
panniculus.49 Because of their distinct histological patterns, Impetigo is a superficial pustular dermatitis, most commonly
these two categories will be discussed in detail in this and the caused by coagulase-positive staphylococci, such as S. pseudin-
next sections. termedius in dogs or S. aureus in other species.98 Dogs, cats,
cattle, goats, and sheep are the most commonly affected species.
Lesions usually occur at the time of puberty and are nonpruritic,
Superficial Pyoderma nonpainful, and frequently heal spontaneously.56 Predisposing
Superficial pyoderma, also clinically known as bacterial fol- factors are a moist environment, skin abrasions, parasitism,
liculitis, is one of the most common skin diseases in dogs.49 It stress, or poor nutrition.56,98 Patients present with small, ery-
involves the penetration of bacteria through the epidermis and thematous papules and pustules affecting the interfollicular epi-
invasion into the follicular ostia, leading to folliculitis. The pri- dermis.56 Lesions occur most often in the axillary and inguinal
mary pathogen associated with this condition is Staphylococcus regions in dogs. In kittens, areas that are in contact with the
spp., primarily S. pseudintermedius, followed by S. interme- mouth of the queen during transportation are most affected.56
dius, S. delphini, and S. schleiferi (S. coagulans—coagulase Cows, does, and ewes have lesions mainly on the base of the
positive, and S. schleiferi—coagulase negative),10 although teats and intermammary sulcus of the udder, ventral abdomen,
other bacterial species can also be associated with this condi- perineum, vulva, medial thighs, and ventral tail.56,98 Pustules are
tion.38,56 Staphylococci are normal commensals in the skin of fragile and frequently rupture, producing a honey-colored crust
healthy dogs,79 and it is therefore suggested that underlying over a shallow erosion (Supplemental Fig. S1e).38,56
factors related to the host may be the primary cause of bacterial Bullous impetigo is a more severe form of the disease that
pyoderma. In fact, healthy canine skin harbors a significantly can also affect adult dogs. Pustules are more extensive and
diverse bacterial community, while dogs with pyoderma lesions span several hair follicle ostia. Patients with impetigo often
have a loss of diversity and a higher relative abundance of have underlying conditions, such as iatrogenic or naturally
Staphylococcus spp.66 Likewise, allergic dogs have increased occurring hyperglucocorticoidism, diabetes mellitus, or
Faccin et al 799

Figure 2. Bacterial diseases affecting the epidermis. (a) Superficial pyoderma, dog. Pustules and epidermal collarettes surrounded by
erythema in the axillary region. (b) Superficial pyoderma, dog. Neutrophils infiltrate and aggregate within the epidermis forming superficial
pustules with superficial bacterial colonies (arrow), that may extend into the follicular ostia. Hematoxylin and eosin (HE). (c) Impetigo,
dog. Intact subcorneal pustule filled with neutrophils. Note shallow erosion of the underlying epidermis. Higher magnification of the cells
in the subcorneal pustule is seen in (d) and (e). HE. (d) Impetigo, dog. Few acantholytic cells (arrows) are within pustules, detaching from
the underlying epidermis. HE. (e) Impetigo, dog. Coccoid bacteria (arrows) are within neutrophilic inflammation. HE. (f) Dermatophilosis,
calf. The skin is covered with dry and domed thickly adherent crusts. (g) Dermatophilosis, horse. Marked epidermal hyperplasia covered
with a thick crust with inflammatory cells and necrotic debris. HE. (h) Dermatophilosis, horse. Parallel rows of coccoid bodies with a typical
“railroad track” appearance within the crust (arrows, inset). HE. (i) Dermatophilosis, horse. Gram-positive bacteria within the lumen of
a hair follicle. Gram stain. (j) Exudative epidermitis or greasy pig skin disease, piglet. Thick crusts cover the face and ears of the piglet on
the left, and a greasy and brown exudate with multifocal crusts covers the entire body of the piglet on the right. (k) Exudative epidermitis
or greasy pig skin disease, piglet. Nonintact neutrophilic pustules forming extensive and thick serocellular crusts overlay the hyperplastic
epidermis. Moderate edema is in the superficial dermis. HE. (l) Exudative epidermitis or greasy pig skin disease, piglet. Aggregates of gram-
positive coccoid bacteria (arrows) are within the serocellular crust, which contains numerous degenerative neutrophils. Gram stain.

hypothyroidism.38,56,98 Bacteria other than staphylococci may bacteria are within intact pustules (Fig. 2e), which can be high-
play a role, such as E. coli or Pseudomonas.56 lighted with a Gram stain. Specimens with nonintact pustules
The main histologic changes are subcorneal pustules filled can be a challenge, as secondary bacterial infections can occur
with neutrophils that are not associated with hair follicles (Fig. in patients with pemphigus foliaceus.38
2c).38,56,98 Bacterial toxins cleave intercellular adhesion mole-
cules (desmoglein 1) leading to keratinocyte detachment and
Dermatophilosis
formation of acantholytic keratinocytes, which needs to be dif-
ferentiated from pemphigus foliaceus (Fig. 2d).38,56,98 In impe- Dermatophilosis, also known as streptotrichosis, rain rot, or
tigo, fewer acantholytic keratinocytes are seen and cocci rain scald, is caused by Dermatophilus congolensis, a
800 Veterinary Pathology 60(6)

gram-positive facultative anaerobic bacterium. The disease is crusting with large numbers of neutrophils, exfoliated stratum
common in tropical and subtropical climates. Cattle are most corneum (Fig. 2k), and numerous colonies of gram-positive
often affected. In temperate climates, goats and sheep are com- coccoid bacteria (Fig. 2l).28,67 In chronic cases, the crusts are
monly affected. Occasional infection occurs in horses and cam- composed of marked orthokeratosis and parakeratosis; the
els.56,84,98 Dermatophilosis can cause major economic losses as underlying epidermis is acanthotic with hyperplastic rete pegs;
the disease can become generalized and animals become seri- and the dermis is infiltrated with histiocytes, lymphocytes, and
ously ill and udder or teat lesions can hinder the suckling of plasma cells.28,67
calves.56,84 The dorsum and distal extremities are most com-
monly affected, and consist of papules, pustules, and domed,
adherent crusts (Fig. 2f).56,98 There are two main predisposing Bacterial Diseases Affecting Hair
factors: wet conditions/prolonged wetting (hence called also Follicles and Adjacent Dermis
“rain rot” or “rain scald”) and trauma to the skin (eg, due to
ticks, insects, or UV damage).56,84,98 Softening of stratum cor-
Deep Folliculitis, Furunculosis, and Pyoderma
neum and dissolving of lipid film after prolonged rain or trauma Deep pyodermas often develop secondary to traumatic furun-
to the skin makes it easier for zoospores/coccoid bodies to culosis, actinic comedones, and even demodicosis; these can be
overcome the skin barrier. Zoospores then produce branching a sequela of superficial bacterial folliculitis.38 Some forms of
filaments that infiltrate into the epidermis and outer root sheath deep pyoderma are clinically or histologically distinct, and
of the hair follicles. After penetration, keratinocytes begin to therefore categorized separately, such as the German Shepherd
cornify and neutrophils accumulate and inhibit further invasion pyoderma, postgrooming furunculosis, canine acne, and oth-
of the organisms. Then the cycle repeats, resulting in layered, ers.38 A detailed discussion of each of these entities is beyond
thick crusts.56,98 D congolensis may be more difficult to grow in the scope of this article. However, they share some common
culture than other bacteria and can be zoonotic.84,98 pathological features that will be covered below.
The histologic hallmark of dermatophilosis is a thick crust Staphylococcus spp. are the major pathogens associated with
with alternating layers of orthokeratosis and parakeratosis, and folliculitis, furunculosis, and deep pyoderma. However, other
inflammatory cells and necrotic debris (Fig. 2g). The typical types of bacteria, such as Streptococcus spp.,23 Proteus spp.,
“railroad track” bacteria consist of parallel rows of coccoid Pseudomonas spp., E. coli,38 Bacillus spp., Corynebacterium
bodies seen within these crusts (Fig. 2h). Gram stain is often spp., and Pasteurella multocida,56 have also been isolated.
helpful to highlight typical gram-positive bacteria within crusts Mixed bacterial infections are common.42 S. pseudintermedius
(Fig. 2i). There may be intraepidermal neutrophilic micropus- and S. schleiferi are the two most prevalent staphylococcaceae
tules or subcorneal pustules, and suppurative, luminal folliculi- isolated from dogs. Both can develop methicillin resistance,
tis. Inflammation in the dermis is usually mild.56,98 which is a major issue in the treatment of this condition.42 The
zoonotic potential of multidrug-resistant bacteria is another
serious concern, and although uncommon and transient,29 own-
Exudative Epidermitis
ers of dogs with methicillin-resistant S. pseudintermedius and
Exudative epidermitis (EE), or greasy pig disease, is a well- veterinarians may become carriers of multidrug-resistant staph-
recognized bacterial proteolytic acantholytic dermatosis of pig- ylococcal organisms.25,73,96
lets and weaners.28,67 The main cause of EE is the bacterial In general, these infections are initially centered within hair
strains of Staphylococcus hyicus that express exfoliative toxins follicles, leading to a crusted papule and fragile transient pus-
known as ExhA, ExhB, ExhC, ExhD, SHETA, and SHETB.30 tules. Affected hair follicles lose the hair shafts, causing patchy
Methicillin-resistant strains of S aureus (MRSA),94 S sciuri,16 progressive alopecia. As lesions become more severe, ulcer-
and S chromogenes1 have also been associated with EE in pigs. ation and suppurative or serosanguinous exudate are seen, with
Although S. hyicus is considered a commensal bacterium on the formation of crusts (Fig. 3a). When furunculosis occurs, the
the conjunctiva, snout, ear, and vagina of pigs, it enters the epi- skin becomes nodular and dark red, with draining tracts, ulcers,
dermis through abrasions.27 Desmoglein-1 is the target protein severe edema (Fig. 3b), and occasional hemorrhagic bullae. In
of the exfoliative toxins, which lyse the extracellular domain of severe cases, the animal may present with reactive lymphade-
this cadherin family glycoprotein.30 The first lesions of EE are nomegaly, fever, and anorexia.56
red and moist and start around the eyes, mouth, and ears; in the The histological changes vary greatly, depending on the
axilla and groin; and in areas of trauma. Lesions coalesce and duration of the infection and the presence of furunculosis. In
quickly form a thick, odoriferous, greasy, brown exudate the initial stages, neutrophilic folliculitis predominates (Fig.
throughout the entire skin, herein called greasy pig disease 3c, d), which may result in hair follicle distention and rupture
(Fig. 2j).28 Dehydration and anorexia may lead to death. In (Fig. 3e), leading to a foreign body-type reaction to the free
recently weaned pigs, lesions are confined to the head, and in keratin and hair shafts in the adjacent dermis (Fig. 3f). At this
adults, on the back and flanks. Histologically, the earliest stage, a pyogranulomatous reaction is more commonly appre-
lesions are subcorneal vesicles and neutrophilic pustules with a ciated.38,56 In the interfollicular dermis, aggregates of neutro-
few acantholytic keratinocytes that may involve hair follicles. phils and hemorrhage can form hemorrhagic bullae. Eosinophils
As the lesions progress, there is superficial serocellular may be present if lesions are accompanied by ectoparasites or
Faccin et al 801

Figure 3. Bacterial diseases affecting hair follicles and adjacent epidermis. (a) Deep pyoderma, dog. Crusts, ulcers, and alopecia at the
dorsocaudal region. (b) Deep folliculitis, furunculosis, and pyoderma, dog. Multifocal to coalescing raised alopecic papules/nodules with
multifocal exudation of serosanguineous material in the chin and lips. (c) Deep folliculitis, dog. The follicular lumen is dilated with abundant
keratin, and there is perifollicular hypercellularity to due to numerous inflammatory cells. Adjacent sebaceous glands are irregularly
hyperplastic. Hematoxylin and eosin (HE). (d) Deep folliculitis, dog. Closer view of (c) showing numerous coccoid bacteria (arrows) within
the follicular lumen surrounding a hair shaft. HE. (e) Deep folliculitis, furunculosis, and pyoderma, dog. Subgross image demonstrating
inflammation centered around and within a hair follicle (arrow) and extending into the deep dermis. The epidermis is hyperplastic and
covered with crusts on the right margin. HE. (f) Deep folliculitis, furunculosis, and pyoderma, dog. Inflammation surrounds free keratin
(arrowhead) and a single free hair shaft (arrow), with abundant fibrosis on the right lower corner. HE. (g) Post-grooming furunculosis, dog.
Ruptured hair follicle with an “exploded” appearance within the infundibular region (arrow), surrounded by inflammation and hemorrhage.
HE. (h) Interdigital furunculosis and pododermatitis, dog. In both feet, the interdigital region is swollen and erythematous, forming raised
nodules (arrows). (i) Interdigital furunculosis and pododermatitis, dog. Subgross image showing markedly dilated follicles with abundant
keratin and surrounded by inflammatory infiltrates. HE.

allergic conditions. Hemorrhage and fibrosis are variable. Just can evolve into systemic infection, leading to death by sepsis.
like in superficial pyodermas, bacteria are not always seen even In these cases, the bacteria and fibrin thrombi are seen in the
with the use of special stains,56 as a high colony-forming unit liver, lung, spleen, lymph nodes, brain, kidneys, and other
count is needed for bacteria to be seen histologically.39,100 organs.13,99
In dogs3,13 and cats,99 cases of severe folliculitis, furunculo-
sis, and deep pyoderma have been recently attributed to
Postgrooming Furunculosis
Burkholderia cepacia (formerly known as Pseudomonas cepa-
cia) associated with contaminated devices, shampoos and Postgrooming furunculosis is a severe type of deep folliculitis,
grooming products, disinfectants, ear-cleaning solutions, and furunculosis, and pyoderma associated with vigorous groom-
contaminated surgical cold sterile solution.3,13 Erythematous to ing with contaminated bathing products and instruments.38 The
hemorrhagic papules, plaques, nodules, alopecia, crusts, and most common associated bacterium is Pseudomonas aerugi-
ulcers with draining tracts are primarily in the dorsum, trunk, nosa,37,75,92 but S. pseudintermedius (including methicillin-
and upper limbs, and less commonly in the face and inguinal resistant strains), S. epidermidis, Enterobacter cloacae,
region. Histologically, there is severe pyogranulomatous der- S. hominis, Klebsiella oxytoca, B. cepacia, Proteus sp., E. coli,
matitis with folliculitis and furunculosis in the dermis and pan- and Serratia marcescens have also been reported.13,14,37 These
niculus. Giemsa and Gram stains highlight gram-negative rods bacteria have been isolated from shampoos, electric clipper
inside macrophages and free within the tissue.3,13 The disease blades, clipper handles, and grooming leashes.34,74
802 Veterinary Pathology 60(6)

The lesions have an acute onset of 2 days after grooming or bacterial pseudomycetoma. The most common agent is S.
water immersion, but they may take up to 7 days to develop. aureus; however, other bacteria such as Streptococcus spp.,
Hemorrhagic crusts, papules, pustules, pinpoint ulcers or drain- Pseudomonas spp., E. coli, Proteus spp., and Pasteurella spp.
ing tracts, and nodules or hemorrhagic furuncles commonly have been isolated.71 The infection most often occurs as a result
affect the dorsum of the neck and trunk in the majority of of trauma, such as lacerations, surgery, or punctures, with
patients,14 as they are application sites of contaminated groom- immunosuppressed individuals being more susceptible.
ing products.37 Lesions can also occur in the inguinal region, The subcutis is most often affected; however, multiple organs
limbs, and abdomen.14 Alopecia is also noted as the severity can be involved.57 Multiple firm, nonpruritic subcutaneous nod-
increases.38 Major clinical signs include pain, fever, and inap- ules often have draining tracts and ulcers.85 The center of the
petence.14 Rarely, the disease can evolve into sepsis and death, nodules contains purulent material and white granules.44 In
especially if it involves multidrug-resistant bacteria.75 horses, widespread infection follows the lymphatic vessels.85
Histologically, the hair follicles are ruptured, as if they had Resolution of localized lesions often requires complete surgical
“exploded” (Fig. 3g),38 with severe suppurative furunculosis excision, as antimicrobials alone are not effective in clearing
associated with fragmented hair shafts and keratin, usually these infections.57 Histologically, these nodules are character-
within the superficial dermis. Other findings include hemor- ized by pyogranulomatous inflammation with numerous multi-
rhage, edema, and congestion.14,38 Bacteria are not always vis- nucleated cells (Fig. 4a). Clusters of gram-positive coccoid
ible, and Gram stain may be negative.14 Given the severity of bacteria, often observed within the center of these pyogranulo-
this disease, the lesions tend to be biopsied in its acute stage; mas, are surrounded by deeply eosinophilic club-like material
therefore, chronic granulomatous furunculosis and scarring are forming the Splendore–Hoeppli reaction (Fig. 4b), which cor-
unusual.38 responds to the white grains observed macroscopically.44

Interdigital Furunculosis and Pododermatitis Nocardiosis


Pododermatitis with interdigital furunculosis, also known as In companion animals, Nocardia spp. can cause chronic skin
pedal furunculosis, interdigital bullae, and interdigital pyo- infections, in addition to frequently infecting the lungs and
granuloma, is a deep bacterial infection almost always associ- pleura, whereas in cows it is more commonly responsible for
ated with an underlying factor.42 It is considered a subgroup of mastitis. These organisms are ubiquitous in the environment,
deep pyoderma38 that affects the interdigital area of dogs, espe- being found in organic matter in soil, water, and plants that can
cially short-coated breeds.42 Initially, the condition starts with be inoculated into the skin via puncture wounds. Nocardia spp.
single or multiple nodules of interdigital furunculosis with are facultative intracellular aerobic filamentous bacteria. The
occasional hemorrhage and ulceration, forming draining tracts most common species infecting the skin are from the Nocardia
(Fig. 3h). The underlying causes of furunculosis can be trauma, asteroides complex, which results in cutaneous nodules that
excessive licking, demodicosis, atopic dermatitis, or allergic may become ulcerated and form draining tracts (Fig. 4c). The
diseases that cause pruritus, or conditions that alter weight- infections can be refractory to conventional therapy, and cuta-
bearing.2,61 Most common bacterial species involved include neous infections may be complicated by the invasion of adja-
S. pseudintermedius, Streptococcus spp., E. coli, Klebsiella spp., cent tissues, leading to pulmonary infections and even
and Pseudomonas spp.42,61 Some lesions resolve spontaneously, disseminated disease, especially in immunosuppressed ani-
while others wax and wane, or can persist indefinitely.42 mals.78 Histologically, nodular to diffuse pyogranulomatous
Clinically, the interdigital nodules contain purulent or case- inflammation in the dermis and subcutis (Fig. 4d) aggregates
ous material with numerous hair fragments when expressed.24,42 around tangled colonies of beaded and filamentous bacteria
Other areas of the body are usually not affected.24 Histologically, (Fig. 4e).44 It is uncommon for these organisms to form tissue
the dermis contains multifocal, nodular to diffuse pyogranulo- grains or to be surrounded by the Splendore–Hoeppli reaction.
matous dermatitis with furunculosis (Fig. 3i). With chronicity, Histologically, Nocardia spp. are gram positive and partially
fibrosis is also appreciated. Special stains are usually negative acid-fast positive (Fig. 4f), allowing it to be distinguished from
for infectious agents, unless a secondary bacterial infection Actinomyces spp., which are negative with acid-fast stains. A
develops, and culture and antimicrobial sensitivity tests are modified acid-fast stain like Fite-Faraco, instead of Ziehl-
recommended in these cases.42 Nielsen, may be more beneficial to confirm Nocardia infection,
as it is less susceptible to decolorization during processing.38,44
An issue that is often faced by pathologists is that the bacterial
Bacterial Diseases Primarily Involving
colonies in tissues may be sparse and multiple sections may be
the Dermis and Panniculus needed to be evaluated for organisms to be found.
Botryomycosis
Botryomycosis is a chronic deep dermatitis that occurs in sev-
Actinomycosis
eral species, including dogs, cats, pigs, cattle, horses, labora- Actinomyces spp. can be normally found in the oral cavity, and
tory animals, and humans. The disease is commonly known as cutaneous infections are usually a result of bite wounds
Faccin et al 803

Figure 4. Bacterial diseases primarily involving the dermis and deep panniculus. (a) Botryomycosis, dog. Pyogranulomatous inflammation
(inset) with central clusters of coccoid bacteria surrounded by deeply eosinophilic club-like material (Splendore–Hoeppli reaction).
Hematoxylin and eosin (HE). (b) Botryomycosis, dog. Numerous gram-positive cocci surrounded by Splendore-Hoeppli reaction. Gram
stain. (c) Nocardiosis, dog. Nodule affecting the hind limb digit with ulceration and hemorrhage. (d) Nocardiosis, cat. Subgross image of a
locally extensive nodular area of inflammation extending from the mid dermis into the deep dermis and panniculus. HE. (e) Nocardiosis,
cat. The organisms aggregate within the center of the inflammatory reaction as serpiginous colonies of beaded and filamentous bacteria
(inset). (f) Nocardiosis, cat. Nocardia spp. are acid-fast bacteria. Fite-Faraco. (g) Actinomycosis, dog. Confluent inflammation extending from
the superficial dermis to the deep dermis and panniculus with central hemorrhage. HE. (h) Actinomycosis, dog. Colonies of filamentous
bacteria (inset) surrounded by Splendore-Hoeppli material and numerous multinucleated giant cells and neutrophils. HE. (i) Actinomycosis,
dog. Gram-positive filamentous bacteria (inset) surrounded by the Splendore–Hoeppli material. Gram stain. (j) Pseudomonas luteola, cat.
Neutrophils and scattered epithelioid macrophages admixed with 1- to 3-μm-diameter oval organisms with a clear capsule (arrows, inset).
HE. (k) Pseudomonas luteola, cat. Elongated bacteria have an approximately 3-μm periodic acid-Schiff (PAS)-positive capsule (arrows). (l)
Necrotizing fasciitis, dog. Medial aspect of the leg with overlying skin removed showing necrotic and hemorrhagic subcutaneous tissue.

or penetrating injury, occurring most often in hunting dogs or (Fig. 4g, h). Both organisms are gram positive (Fig. 4i); how-
animals that have access to outdoor environments. Small ani- ever, Actinomyces is acid-fast negative. The Splendore–Hoeppli
mals will often present with cutaneous or subcutaneous nod- reaction is more commonly observed in Actinomyces, but infre-
ules, as well as deep cellulitis that may become ulcerated and quent in Nocardia infection.38,44 A similar pattern may also be
fistulate.42 The intralesional colonies can occasionally be seen seen in botryomycosis; however, the latter will have intrale-
clinically as yellow-tan sand-like granules. sional cocci bacteria instead of filamentous bacteria. Multiple
Actinomyces spp. cause large and often confluent areas of lesions are recommended to be biopsied, as these organisms
pyogranulomatous inflammation predominantly composed of can be difficult to find in histological specimens, and multiple
large numbers of neutrophils surrounded by epithelioid macro- deeper sections may be needed for these aggregates of filamen-
phages, similar to those observed in Nocardia infections tous bacteria to be found.38 Rarely, colonies of Actinomyces
804 Veterinary Pathology 60(6)

spp. can form narrow branched hyphae-like filaments in tis- those of the “Terrae” clade are now of the Mycolicibacter
sues,59 a characteristic that is also seen in culture, with the for- genus; the “Triviale” microorganisms belong to the
mation of spore, spore chain, sporangia, and mycelium.48 Mycolicibacillus genus; and the “Abscessus-Chelonae” clade
is now part of the Mycobacteroides genus.40
In the next sections, we will discuss different mycobacterial
Pseudomonas Luteola and mycolicibacterial infections in different animal species,
Pseudomonas luteola is a rare gram negative pathogen using the current nomenclature for each microorganism.
described in cats58 and ferrets.6,55,83 It is usually associated with
septicemia and pyogranulomatous inflammation affecting the
Fast-Growing Mycolicibacterial/Mycobacteroidal
panniculus, pleura, mediastinum, salivary glands, and
lungs.6,55,83 A case report in a cat58 described pyogranulomatous Infections
dermatitis and panniculitis with numerous 1- to 3-μm-diameter Fast-growing mycolicibacterial/mycobacteroidal infections
oval organisms (Fig. 4j) with a 3-μm periodic acid-Schiff are opportunistic infections caused by species of the genera
(PAS)-positive capsule (Fig. 4k). The organism also stains Mycolicibacterium or Mycobacteroides which grow rapidly in
weakly with Grocott’s methenamine silver. Mayer’s mucicar- culture (often in less than 7 days). These bacteria are included
mine is negative. Because of the unusual morphology of the within the Runyon Group IV (Mycolicibacterium smegmatis
microorganisms, P. luteola should be a differential diagnosis complex, M. fortuitum, M. flavescens, M. thermoresistible, and
for other infections, such as leishmaniasis, histoplasmosis, and Mycobacteroides Chelonae-Abscessus complex).53 These
even cryptococcosis. organisms can be found in soil and water throughout the world,
and infections are often the result of traumatic penetration of
Necrotizing Fasciitis these microorganisms into broken skin.38 These organisms
have tropism for lipid, and lesions are most often centered in
Necrotizing fasciitis, also known as flesh-eating disease, is a the subcutaneous tissue.53 In cats, these infections are often
rapidly progressive and potentially life-threatening condition seen in the ventral abdominal region, involving the inguinal fat
characterized by deep necrotizing panniculitis and fasciitis.93 It pads.38
is usually caused by bacterial inoculation to the deep tissues, Clinically, the infection may lead to cutaneous and subcuta-
such as cat scratches,4 vaccinations,35,93 or after traumatic inju- neous abscesses, which may fistulate and form draining tracts
ries,11 but the source of the infection might not always be (Fig. 5a, Supplemental Fig. S1f). Histologically, multifocal to
apparent.97 In dogs, it is most commonly associated with coalescing pyogranulomatous panniculitis often extends to and
Streptococcus canis, S. pseudintermedius, E. coli, S. zooepi- involves the dermis and panniculus (Fig. 5b). The inflamma-
demicus, and P. multocida.4,35,93,97 In cats, this condition has tion is composed of aggregates of neutrophils surrounded by
been associated with S. canis, Prevotella bivia, S. pneumoniae, large numbers of epithelioid macrophages mixed with fewer
and Acinetobacter baumannii.11,22,91,93 Fournier’s gangrene is a lymphocytes and plasma cells. Neutrophils and macrophages
type of necrotizing fasciitis that affects the genital, perianal, often surround clear, empty lipid vacuoles (lipid from broken
and perineal regions. This entity has been described in a cat, adipocytes), and the visualization of this feature justifies the
caused by Enterococcus faecium, S. epidermidis, and E. coli.8 use of special stains. Thin and elongated entangled bacilli to
Affected animals are usually lethargic with fever and pain, short filamentous bacteria may be lodged within the lipid vacu-
and can present ecchymosis and swelling of the affected areas oles (Fig. 5c). Fite-Faraco acid-fast stain is preferred to identify
(Fig. 4l). The lesion can progress to the formation of hemor- these organisms, and these may also stain with Grocott’s
rhagic bullae and skin necrosis. Histologically, severe necrosis methenamine silver.38 The main challenge in the histological
and suppurative inflammation involve the dermis, panniculus, diagnosis of this infection is that the organisms may be difficult
fascia,11,93,97 and muscles,91 occasionally reaching the bone, to find histologically, even with the use of special stains. The
causing osteomyelitis93 and involving joints.22 Blood vessels lesions can be very similar and must be differentiated from
are usually necrotic, causing thrombosis and ischemia, with cases of sterile pyogranulomatous dermatitis and panniculitis.
subsequent dermal necrosis.4,93 The condition can rapidly prog- Thus, direct smears and culture must be performed prior to rul-
ress to septicemia, affecting multiple internal organs.91 ing out this infection and considering lesions of this nature to
be sterile.
Mycobacterial and Mycolicibacterial Infections
Slow-Growing Mycobacterial Infections
Based on the extensive phylogenomic analysis, the genus
Mycobacterium has been recently emended and four new gen- Slow-growing mycobacterial infections result in cutaneous
era were created to accommodate former members. Therefore, nodules that may be caused by the tuberculous agents, including
Mycobacterium should only be used for microorganisms of the Mycobacterium tuberculosis and M. microti or nontuberculous
“Tuberculosis-Simiae” complex, which includes all the major agents, including Mycobacterium avium, M. genavense, M.
human pathogens. Microorganisms that belong to the clade xenopi, and M. ulcerans. These organisms are fastidious, taking
“Fortuitum-Vaccae” now belong to the genus Mycolicibacterium; 4–6 weeks to grow and often failing to grow in culture.52
Faccin et al 805

Figure 5. Bacterial diseases primarily involving the dermis and deep panniculus, mycobacterial infections. (a) Fast-growing Mycolicibacterium/
Mycobacteroidal infection, cat. Classical clinical appearance of fast-growing Mycolicibacterium/Mycobacteroidal infection with formation of
large draining tracts, ulcers, and exudation. Courtesy of Dr. Adam Patterson. (b) Fast-growing Mycolicibacterium/Mycobacteroidal infection,
cat. Subgross image of multifocal to coalescing granulomas extending from the deep dermis and effacing the panniculus. Hematoxylin and
eosin (HE). (c) Fast-growing Mycolicibacterium/Mycobacteroidal infection, cat. Numerous tangled bacilli (black arrow) are within a central
space (lipid), surrounded by neutrophils and epithelioid macrophages. HE. (d) Mycobacterium avium, cat. Sheets of epithelioid macrophages
infiltrate and efface the dermis. HE. (e) M. avium, cat. Numerous acid-fast elongated bacteria (arrows) are within the cytoplasm of
epithelioid macrophages. Fite-Faraco. (f) Canine leproid granuloma, dog. Bilateral, multifocal to coalescing raised nodules on the ear pinnae.
(g) Canine leproid granuloma, dog. Subgross image of nodular lesion extending from the superficial to deep dermis and elevating the
epidermis. HE. (h) Canine leproid granuloma, dog. Epithelioid macrophages are mixed with lymphocytes and neutrophils. HE. (i) Canine
leproid granuloma, dog. Scattered acid-fast elongated bacteria (arrows, inset) are within the cytoplasm of macrophages. Fite-Faraco.

M tuberculosis, which poses a significant public health risk, infections often requires molecular assays, as these organisms
rarely causes lesions in the skin of cattle, dogs, cats, and horses. often fail to grow in culture. In dogs, miniature Schnauzers and
Of these animal species, only cats are more likely to have cuta- Basset hounds are particularly predisposed to infections with the
neous lesions, whereas the other species likely develop pulmo- M. avium complex. Miniature Schnauzers have been identified
nary or alimentary infections. Cutaneous infections are to have an inherited defect in CARD9, a molecule that plays a
characterized by plaques, nodules, or abscesses that form role in innate immunity, which makes them more susceptible to
draining tracts and may involve the head and limbs. It is com- M avium infection.32 The nontuberculous slow-growing
mon for these patients to have systemic disease with fever and Mycobacterium spp. Are primarily distributed within the dermis,
anorexia. Histologically, these lesions form pyogranulomas and patients present with single or multiple dermal masses. The
with central necrosis and mineralization surrounded by multi- nodules may fistulate, forming a draining tract, and lymph nodes
nucleated cells and epithelioid macrophages. Scattered organ- may be involved.38 In immunosuppressed individuals, these
isms are observed within the center of these granulomas.56 lesions may become disseminated. Histologically, granuloma-
Although less concerning than the tuberculous Mycobacterium tous to pyogranulomatous inflammation is characterized by
spp., many of the nontuberculous slow-growing Mycobacterium sheets of epithelioid macrophages with few scattered multinu-
spp. may also pose public health risks, especially in immuno- cleated giant cells and neutrophils (Fig. 5d). Large numbers of
compromised individuals.32 Cats are one of the main species bacteria are often seen in the cytoplasm of epithelioid macro-
affected by these infections, with lesions mimicking those seen phages with acid-fast stains, especially for lesions caused by the
in feline leprosy syndrome. Differentiation between these M avium complex (Fig. 5e).
806 Veterinary Pathology 60(6)

Canine Leproid Granulomas The third presentation is associated with Candidatus


“Mycobacterium lepraefelis” infection, which results in a much
This condition is mainly seen in short-coated breed dogs, espe- more severe presentation of feline leprosy, where the organ-
cially Boxers.51 Patients present with nodules on the ear mar- isms may become disseminated.62 This organism has been
gins (Fig. 5f), and the feet occasionally affected. It is speculated identified in Australia and New Zealand, and one case was
that these infections may be transmitted by insect bites due to identified in British Columbia, Canada. This disease affects
the predilection for sparsely haired areas. Documented out- middle-aged to older, preferably male, cats with outdoor access.
breaks among related and/or closely housed individuals also Patients present with widespread cutaneous lesions, which can
suggest the transmissibility of this condition.89 Patients can be followed by systemic involvement. Due to the progressive
recover with complete surgical excision of lesions, and it may and systemic involvement, this infection may lead to death or
be self-limiting in some immunocompetent individuals.51 The result in euthanasia.
causative agent has yet to be identified, but it appears to be a Histologically, these Mycobacterium spp. may cause lepro-
member of the Mycobacterium genus15,51 that fails to grow in matous or tuberculoid leprosy in cats. In lepromatous leprosy,
culture media. Studies using similar methods of 16S rRNA gene sheets of epithelioid macrophages admixed with neutrophils,
sequencing have determined a high degree of identity (99– plasma cells, and lymphocytes are seen within the dermis and
100%) among samples from similarly described cases in panniculus, with large numbers of organisms observed within
Australia, Brazil, Ireland, New Zealand, and the USA.26,89 the cytoplasm of macrophages. In tuberculoid leprosy, dermal
Ongoing genomic investigations recently performed by our to subcutaneous granulomas with central caseous necrosis are
group show this is a novel Mycobacterium species, most likely observed, and low numbers of organisms are seen within
within the M genovense group. necrotic areas, similar to lesions caused by tuberculosis.
Cutaneous infection caused by this organism leads to the Lepromatous leprosy was the most common presentation in
formation of confluent pyogranulomatous inflammation (Fig. cases caused by Candidatus “M. lepraefelis.”
5f) with sheets of epithelioid macrophages admixed with neu-
trophils, lymphocytes, and plasma cells (Fig. 5h). Sparse, 2–5
µm acid-fast positive bacilli can be seen within the cytoplasm Farcy
of epithelioid macrophages (Fig. 5i). The organisms are more This is a chronic skin disease in cattle that causes lymphangitis
likely to stain with Fite-Faraco acid-fast stain. and dermatitis that is primarily distributed within Sub-Saharan
Africa. The causative agents include Mycolicibacterium sene-
Feline Leprosy galensis and Mycolicibacterium farcinogenes. The infection
can be zoonotic, although only rare cases have been reported in
Feline leprosy is often seen in cats that have access to outdoor humans. However, the main public health concerns related to
environments, and this condition can be divided into three dif- farcy are because lesions can mimic those seen in cattle with
ferent presentations, which are caused by different pathogens.62 tuberculosis. It is believed that farcy enters the skin via abra-
One of the most common presentations is caused by sions and wounds. Tick transmission may also play a role due
Mycobacterium lepraemurium, which is seen in many coun- to the geographic distribution of this disease, as well as the fact
tries, especially in coastal regions.64 M. lepraemurium can be that breeds resistant to ticks are also resistant to farcy. The bac-
found in rats, and the development of lesions is believed to be teria initially penetrate the subcutaneous tissues resulting in
a result of potential encounters with rodents. It is not a zoonotic cellulitis, invading lymphatics and involving regional lymph
agent, and no direct transmission between cats has been nodes. Clinically, linear nodules with draining tracts and leak-
reported. Few to numerous nodules within the skin and subcu- age of yellow purulent material are the most characteristic
taneous tissues, which may become ulcerated, are seen mainly lesion seen in the chronic phase of this disease. Histologically,
in cats younger than 3 years of age. They are primarily on the classic granulomas with central necrosis and mineralization
head and limbs, with fewer nodules involving the body and tail, surrounded by macrophages and multinucleated giant cells are
and, only infrequently, the disease can be generalized. The observed. Only rare to few acid-fast organisms may be seen
infection has an indolent course, and is associated with a good histologically, although oftentimes these may be missed due to
prognosis even in untreated patients with persistent disease, but the paucity of bacilli within histological sections.41
without the involvement of internal organs.
The second presentation of feline leprosy has been attrib-
uted to a novel Mycobacterium within the M. simiae complex,
Glanders
Candidatus “M. tarwinense,” with lesions seen in the head, Glanders is a zoonotic infection seen in horses, mules, and don-
especially involving periocular tissues.63 It is believed that cats keys caused by Burkholderia mallei. This agent is highly con-
acquire this infection during fights with other cats, or from tagious and can be fatal in humans. It is included as one of the
fights or hunting prey species. This condition has an indolent category B bioterrorism agents by the Centers for Disease
course with a favorable prognosis in most cases. This novel Control and Prevention. The disease has been eradicated in
pathogen is almost entirely confined to the Victoria region in many countries, although scattered outbreaks are still seen in
Australia. some regions around the world. Asymptomatic patients and
Faccin et al 807

those during early infection periods can serve as the source of affected.47,98 Clinically, erythema, petechiae, necrosis, ulcer-
infection in other animals. The organisms can invade the skin, ation, and edema are visible. Rickettsia spp. targets the host’s
mucous membranes, and gastrointestinal tract. Infected ani- endothelial cells and causes direct endothelial damage, which
mals may also develop systemic signs including fever, anorexia, results in endothelial proliferation, inflammation, and hemor-
weight loss, and cough. Patients can present with a cutaneous, rhage. Histologically, neutrophilic small vessel vasculitis with
nasal, and/or pulmonary form, with a combination of cutaneous leukocytoclasia, fibrinoid necrosis, and fibrin thrombi are
and pulmonary forms being the most common clinical presen- observed.56,98 Treatment of insufficient duration may lead to
tation in disease outbreaks. The cutaneous lesions of glanders disease relapse.47
are similar to those seen in farcy in cattle, and “farcy” is also a
term used to describe glanders in affected animals. Nodular
cutaneous ulcers in a “crate-like” pattern that appears as chains
Lyme Disease
with drainage of serous and purulent exudate are the character- Lyme disease is caused by Borrelia burgdorferi, a gram negative
istic lesions. The linear aspect of the lesions is the result of spirochete, transmitted by Ixodes spp. The disease is described
severe lymphangitis.46 in dogs, horses, and humans. In humans, an expanding ring-
like erythema develops about 1–2 weeks after the tick bite.56
Dogs can have a rash, urticaria, and moist dermatitis.56 In
Bacterial Diseases Causing Vasculitis horses, cutaneous lymphoid hyperplasia, formerly pseudolym-
Erysipelas phoma, has been reported. One reported horse displayed der-
mal papules ranging from 2–7 mm in size across the ventral
Erysipelothrix rhusiopathiae is a gram-positive bacillus,95 aspect of the right masseter.86 Histologically, densely cellular
known to cause several syndromes in pigs, such as septicemia, infiltrates consisting of large, lymphoblastic cells, intermixed
arthritis, vegetative endocarditis, cutaneous vasculitis, and with small, mature lymphocytes are observed. The infiltrate
abortion.69 This pathogen is zoonotic and is reported in a vari- was separated from the epidermis by a Grenz zone.
ety of mammals, birds, reptiles, and invertebrates.95 Wild boars Immunohistochemistry showed a mixed CD3 and CD79a-
are thought to be a reservoir for the bacteria, posing a threat to positive cell population.86 Cutaneous lymphoid hyperplasia
domestic pigs and other species.88 may be a more general reaction of tick bites.
With acute septicemia, the pigs develop cyanotic or ery-
thematous extremities and small papules or large, raised, firm
plaques with characteristic diamond or rhomboid shapes (Fig. Purpura Hemorrhagica
6a). As the disease progresses, the lesions become dry and Purpura hemorrhagica is common in horses and is most com-
darker with a necrotic center, and the skin can be easily peeled monly associated with Streptococcus equi subsp. equi (stran-
from the underlying tissues (Fig. 6b). In severe cases, the ears, gles-associated) and Corynebacterium pseudotuberculosis
tail, and foot can slough due to necrosis.69 infections, or in correlation with vaccinations or other infec-
Histologically, there is marked dermal neutrophilic vasculi- tions, such as Rhodococcus equi, equine influenza virus, or
tis with thrombosis (Fig. 6c), which gives the characteristic equine herpesvirus type 1.77,98 The skin, respiratory tract, or
diamond appearance grossly, with cutaneous necrosis and sup- gastrointestinal tract may be affected. Clinically, there is well-
purative hidradenitis.56 The cutaneous form of erysipelas has demarcated subcutaneous edema on all four limbs, hemor-
also been reported in dogs with alopecia and erythematous rhages in the mucous membranes, and purple macules in the
macules. Histologically, they consisted of neutrophilic vasculi- ventrum, head, and distal limbs.77,98 Systemic signs include
tis and fibrinoid necrosis at all levels of the dermis, mixed with fever, depression, and anorexia. The histologic lesions are an
fibrin, hemorrhage, and edema.54 immune-mediated vasculitis due to antigen-antibody-complex
deposition in vessel walls (type III hypersensitivity reaction)
Rocky Mountain Spotted Fever with fibrinoid necrosis and neutrophilic, leukocytoclastic vas-
culitis. Lesions may progress to ulceration and sloughing of the
Rocky Mountain spotted fever is caused by Rickettsia and is skin.98 Most horses survive the disease with treatment77; how-
transmitted by ticks, mainly by Dermacentor variabilis or D. ever, there may be complications due to dermal necrosis, laryn-
andersoni, Rhipicephalus sanguineus, and Amblyomma sculp- geal edema, thrombophlebitis, glomerulonephritis, and colic.7
tum, and is, therefore, a seasonal disease.47,98 The disease is
most prevalent in North, Central, and South America. Dogs are
especially susceptible to infection and clinical disease, and
Porcine Ear Necrosis Syndrome
dogs may even serve as sentinels for the disease in humans.47 Porcine ear-tip necrosis (ETN) results in progressive loss of the
Fever is a common early clinical sign and develops three to ear helix in the nursery and early-grower pigs.21 Several syn-
seven days after the tick bite. Other clinical signs include leth- onyms have been used for this syndrome over the years, such
argy, anorexia, skin rash, tremors, ocular lesions, thrombocyto- as porcine ear necrosis, ear necrosis syndrome, ulcerative spi-
penia, and leukocytosis. The integumentary, respiratory, central rochetosis of the ear, or streptococcal auricular dermatitis.50
nervous, gastrointestinal, and urogenital systems can be ETN has a global distribution, being most common in countries
808 Veterinary Pathology 60(6)

Figure 6. Bacterial diseases causing vasculitis. (a) Erysipelas, pig. Haired skin with multifocal to coalescing dry and brown plaques with a
necrotic center. (b) Erysipelotrichosis, pig. Cut section of haired skin depicting necrotic surface with underlying areas of hemorrhage and
necrosis in the dermis and panniculus. (c) Erysipelotrichosis, pig. Multifocal vascular thrombosis with scattered neutrophilic infiltrates within
and around blood vessels with overlying acute necrotic epidermis. Courtesy of Dr. David Driemeier and Dr. Paula Pereira. Hematoxylin and
eosin (HE). (d) Porcine ear necrosis syndrome. The ear tips are necrotic with a rim of congestion between the necrotic and viable tissue.

with intensive pig farming, leading to welfare implications.9 Conclusion


Risk factors such as high stocking rate, fully slatted flooring
without straw, high ambient temperature, poor air quality, and The definitive diagnosis of cutaneous bacterial infections still
high humidity have been associated with outbreaks of ETN.72 relies on clinical signs confirmed by bacterial culture and/or
Neither the etiology nor the pathogenesis of ETN has been molecular techniques. However, the recognition of specific his-
fully elucidated. Three hypotheses have been proposed for the tological patterns helps narrow down the differential list to bet-
development of ETN: (a) necrosis of the epidermis due to exfo- ter allocate the resources for ancillary diagnostic tests.
liative toxins of staphylococci, mainly S. aureus; (b) occlusion Therefore, it is crucial for pathologists to recognize the differ-
of capillaries by cold agglutinins or immune complexes pro- ent patterns that bacterial diseases can cause, when special
duced during infection with specific pathogens, such as stains can or cannot be useful, and what are the main anatomi-
Mycoplasma suis; and (c) trauma, such as ear biting or chew- cal structures involved in each case, to provide clinicians a
ing, with β-hemolytic streptococcal infection.21,50 Furthermore, more comprehensive diagnostic report.
Treponema pedis has been detected in the lesions of ETN, with
proposed infection by biting and licking; however, experimen- Acknowledgments
tal infection failed to reproduce the disease.45 The authors acknowledge Drs. Adam Patterson, David Driemeier, and
Initial lesions consist of local erythema, which is often asso- Paula Pereira for gently providing pictures for this paper. They also
ciated with ear biting, followed by necrosis (Fig. 6d) and loss would like to acknowledge the Gastrointestinal Laboratory staff at
of part of the ear pinna if healing occurs. Open wounds are a Texas A&M University for slide scanning.
port of entry for opportunistic pathogens.21 Histologic lesions
include crust formation on the epidermis with granulation tis- Declaration of Conflicting Interests
sue in the dermis and necrosis of the chondrocytes.21 Vasculitis The author(s) declared no potential conflicts of interest with respect to
is not a consistent finding in ETN.72 the research, authorship, and/or publication of this article.
Faccin et al 809

Funding 21. Costa MO, Nosach R, Harding JCS, et al. Partial reproduction of ear-tip
necrosis suggests an infectious, initially bacterial aetiology. Vet Microbiol.
The author(s) received no financial support for the research, author- 2021;262:109246
ship, and/or publication of this article. 22. Costa RS, Costa FB, Barros RR. Antimicrobial treatment of necrotizing fasci-
itis and septic polyarthritis in a cat associated with Streptococcus canis infec-
ORCID iD tion. Vet Dermatol. 2018;29(1):90–91.
Aline Rodrigues Hoffmann https://orcid.org/0000-0001- 23. De Martino L, Nizza S, de Martinis C, et al. Streptococcus constellatus-associ-
ated pyoderma in a dog. J Med Microbiol. 2012;61(Pt 3):438–442.
6148-2531
24. Duclos D. Canine pododermatitis. Vet Clin North Am Small Anim Pr.
2013;43(1):57–87.
References 25. Faires MC, Tater KC, Weese JS. An investigation of methicillin-resistant
1. Andresen LO, Ahrens P, Daugaard L, et al. Exudative epidermitis in pigs Staphylococcus aureus colonization in people and pets in the same household
caused by toxigenic Staphylococcus chromogenes. Vet Microbiol. 2005;105(3– with an infected person or infected pet. J Am Vet Med Assoc. 2009;235(5):540–
4):291–300. 543.
2. Bajwa J. Canine pododermatitis. Can Vet J. 2016;57(9):991–993. 26. Foley JE, Borjesson D, Gross TL, et al. Clinical, microscopic, and molecu-
3. Banovic F, Koch S, Robson D, et al. Deep pyoderma caused by Burkholderia lar aspects of canine leproid granuloma in the United States. Vet Pathol.
cepacia complex associated with ciclosporin administration in dogs: a case 2002;39(2):234–239.
series. Vet Dermatol. 2015;26(4):287–2e64. 27. Foster AP. Staphylococcal skin disease in livestock. Vet Dermatol.
4. Banovic F, Linder K, Boone A, et al. Cat scratch-induced Pasteurella multocida 2012;23(4):342–351.
necrotizing cellulitis in a dog. Vet Dermatol. 2013;24(4):463e107–464658. 28. Frana TS, Hau SJ. Staphylococcosis. Dis Swine. 2019:926–933.
5. Banovic F, Linder K, Olivry T. Clinical, microscopic and microbial character- 29. Frank LA, Kania SA, Kirzeder EM, et al. Risk of colonization or gene transfer
ization of exfoliative superficial pyoderma-associated epidermal collarettes in to owners of dogs with meticillin-resistant Staphylococcus pseudintermedius.
dogs. Vet Dermatol. 2017;28(1):107–1e23. Vet Dermatol. 2009;20(5–6):496–501.
6. Baum B, Richter B, Reifinger M, et al. Pyogranulomatous panniculitis in fer- 30. Fudaba Y, Nishifuji K, Andresen LO, et al. Staphylococcus hyicus exfoliative
rets (Mustela putorius furo) with intralesional demonstration of Pseudomonas toxins selectively digest porcine desmoglein 1. Microb Pathog. 2005;39(5–
luteola. J Comp Pathol. 2015;152(2-3):114–118. 6):171–176.
7. Bertram CA, Ertelt A, Lübke-Becker A, et al. Pathology in practice. J Am Vet 31. Gallo RL, Nakatsuji T. Microbial symbiosis with the innate immune defense
Med Assoc. 2019;255(2):173–176. system of the skin. J Invest Dermatol. 2011;131(10):1974–1980.
8. Berube DE, Whelan MF, Tater KC, et al. Fournier’s gangrene in a cat. J Vet 32. Ghielmetti G, Giger U. Mycobacterium avium: an emerging pathogen for
Emerg Crit Care San Antonio. 2010;20(1):148–154. dog breeds with hereditary immunodeficiencies. Curr Clin Microbiol Rep.
9. Blömke L, Volkmann N, Kemper N. Evaluation of an automated assessment 2020;7(3):67–80.
system for ear and tail lesions as animal welfare indicators in pigs at slaughter. 33. Gortel K. Recognizing pyoderma: more difficult than it may seem. Vet Clin
Meat Sci. 2020;159:107934 North Am Small Anim Pr. 2013;43(1):1–18.
10. Bloom P. Canine superficial bacterial folliculitis: current understanding of its 34. Gould AP, Coyner KS, Trimmer AM, et al. Recovery of meticillin-resis-
etiology, diagnosis and treatment. Vet J. 2014;199(2):217–222. tant Staphylococcus species from pet-grooming salons. Vet Dermatol.
11. Brachelente C, Wiener D, Malik Y, et al. A case of necrotizing fasciitis with 2020;31(4):262-e60.
septic shock in a cat caused by Acinetobacter baumannii. Vet Dermatol. 35. Greijdanus-Van Der Putten SW, Vos JH, Duvekot JR, et al. [Postvaccinal
2007;18(6):432–438. fatal Streptococcus zooepidemicus necrotizing fasciitis in a young dog: a case
12. Bradley CW, Morris DO, Rankin SC, et al. Longitudinal evaluation of the skin report]. Tijdschr Diergeneeskd. 2014;139(9):24–27.
microbiome and association with microenvironment and treatment in canine 36. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol. 2011;9(4):244–
atopic dermatitis. J Invest Dermatol. 2016;136(6):1182–1190. 253.
13. Cain CL, Cole SD, Bradley Ii CW, et al. Clinical and histopathological features 37. Gross T, Crow D. Postgrooming furunculosis in two dogs due to Serratia marc-
of Burkholderia cepacia complex dermatitis in dogs: a series of four cases. Vet escens and Pseudomonas aeruginosa. Vet Dermatol. 2006;17(3):207–220.
Dermatol. 2018;29(5):457–e156. 38. Gross TL, Ihrke PJ, Walder EJ, et al. Skin Diseases of the Dog and Cat: Clinical
14. Cain CL, Mauldin EA. Clinical and histopathologic features of dorsally located and Histopathologic Diagnosis. Wiley; 2005. Published online https://books.
furunculosis in dogs following water immersion or exposure to grooming google.co.in/books?id=VKa2Wo3Wc-kC
products: 22 cases (2005-2013). J Am Vet Med Assoc. 2015;246(5):522–529. 39. Gupta E, Bhalla P, Khurana N, et al. Histopathology for the diagnosis of infec-
15. Charles J, Martin P, Wigney DI, et al. Cytology and histopathology of canine tious diseases. Indian J Med Microbiol. 2009;27(2):100–106.
leproid granuloma syndrome. Aust Vet J. 1999;77(12):799–803. 40. Gupta RS, Lo B, Son J. Phylogenomics and comparative genomic studies
16. Chen S, Wang Y, Chen F, et al. A highly pathogenic strain of Staphylococcus robustly support division of the genus. Front Microbiol. 2018;9:67.
sciuri caused fatal exudative epidermitis in piglets. PLoS One. 2007;2(1):e147. 41. Hamid ME. Epidemiology, pathology, immunology and diagnosis of bovine
17. Chiller K, Selkin BA, Murakawa GJ. Skin microflora and bacterial infections farcy: a review. Prev Vet Med. 2012;105(1–2):1–9.
of the skin. J Investig Dermatol Symp Proc. 2001;6(3):170–174. 42. Hnilica KA, Patterson AP. Chapter 3—bacterial skin diseases. In: Small
18. Christensen GJ, Bruggemann H. Bacterial skin commensals and their role as Animal Dermatology. 4th ed. Elsevier; 2017:45–93.
host guardians. Benef Microbes. 2014;5(2):201–215. 43. Iwase T, Uehara Y, Shinji H, et al. Staphylococcus epidermidis Esp inhib-
19. Cogen AL, Yamasaki K, Muto J, et al. Staphylococcus epidermidis antimicro- its Staphylococcus aureus biofilm formation and nasal colonization. Nature.
bial delta-toxin (phenol-soluble modulin-gamma) cooperates with host antimi- 2010;465(7296):346–349.
crobial peptides to kill group A Streptococcus. PLoS One. 2010;5(1):e8557. 44. Jones T, Hunt D, King W. Veterinary Pathology. 6th ed. Baltimore, MD:
20. Cogen AL, Yamasaki K, Sanchez KM, et al. Selective antimicrobial action Williams & Wilkins; 1997.
is provided by phenol-soluble modulins derived from Staphylococcus 45. Karlsson F, Rosander A, Fellström C, et al. Experimental inoculation of
epidermidis, a normal resident of the skin. J Invest Dermatol. 2010;130(1): Treponema pedis T A4 failed to induce ear necrosis in pigs. Porc Health
192–200. Manag. 2017;3:26.
810 Veterinary Pathology 60(6)

46. Khan I, Wieler LH, Melzer F, et al. Glanders in animals: a review on epi- 68. O’Neill AM, Worthing KA, Kulkarni N, et al. Antimicrobials from a feline com-
demiology, clinical presentation, diagnosis and countermeasures. Transbound mensal bacterium inhibit skin infection by drug-resistant S.pseudintermedius.
Emerg Dis. 2013;60(3):204–221. Elife. 2021;10:e66793.
47. Levin ML, Killmaster LF, Zemtsova GE, et al. Clinical presentation, conva- 69. Opriessnig T, Coutinho TA. Erysipelas. Diseases of Swine. John Wiley &
lescence, and relapse of rocky mountain spotted fever in dogs experimentally Sons; 2019: 835–843.
infected via tick bite. PLoS One. 2014;9(12):e115105. 70. O’Shaughnessy-Hunter LC, Yu A, Rousseau JD, et al. Longitudinal study of the
48. Li Q, Chen X, Jiang Y, et al. Morphological identification of actinobacteria. In: cutaneous microbiota of healthy horses. Vet Dermatol. 2021;32(5):467-e128.
Dhanasekaran D, Jiang Y, eds. Actinobacteria—Basics and Biotechnological 71. Padilla-Desgarennes C, Vázquez-González D, Bonifaz A. Botryomycosis.
Applications. InTech; 2016. Available from: http://dx.doi.org/10.5772/60457. Clin Dermatol. 2012;30(4):397–402.
49. Loeffler A, Lloyd DH. What has changed in canine pyoderma? A narrative 72. Park J, Friendship RM, Poljak Z, et al. An investigation of ear necrosis in pigs.
review. Vet J. 2018;235:73–82. Can Vet J. 2013;54(5):491–495.
50. Malik M, Chiers K, Boyen F, et al. Porcine ear necrosis. Vet J. 2021;271:105655 73. Paul NC, Moodley A, Ghibaudo G. Carriage of methicillin-resistant staphy-
51. Malik R, Love DN, Wigney DI, et al. Mycobacterial nodular granulomas lococcus pseudintermedius in small animal veterinarians: indirect evidence of
affecting the subcutis and skin of dogs (canine leproid granuloma syndrome). zoonotic transmission: methicilln-resistant Staphylococcus pseudintermedius
Aust Vet J. 1998;76(6):403398–403407. in veterinarians. Zoonoses Public Health. 2011;58(8):533–539.
52. Malik R, Smits B, Reppas G, et al. Ulcerated and nonulcerated nontubercu- 74. Perry E, Sutton GA, Haggag L, et al. Pseudomonas aeruginosa isolation from
lous cutaneous mycobacterial granulomas in cats and dogs. Vet Dermatol. dog grooming products used by private owners or by professional pet groom-
2013;24(1):146–53e32. ing salons: prevalence and risk factors. Vet Dermatol. 2022;33(4):316-3e73.
53. Malik R, Wigney DI, Dawson D, et al. Infection of the subcutis and skin of cats 75. Pipe-Martin HN, Peterson TA, Langohr IM, et al. Sepsis and multi-organ dys-
with rapidly growing mycobacteria: a review of microbiological and clinical function associated with postgrooming furunculosis in a dog. Vet Dermatol.
findings. J Feline Med Surg. 2000;2(1):35–48. 2016;27(3):198–1e49.
54. Marshall KR, Walton SA, Boyd M, et al. Erysipeloid lesions caused by 76. Porcellato D, Meisal R, Bombelli A, et al. A core microbiota dominates a rich
Erysipelothrix rhusiopathiae in a dog: clinical and histopathological findings, microbial diversity in the bovine udder and may indicate presence of dysbiosis.
molecular diagnosis and treatment. Vet Dermatol. 2019;30(5):434–e134. Sci Rep. 2020;10(1):21608.
55. Martínez J, Martorell J, Abarca ML, et al. Pyogranulomatous pleuropneu- 77. Pusterla N, Watson JL, Affolter VK, et al. Purpura haemorrhagica in 53 horses.
monia and mediastinitis in ferrets (Mustela putorius furo) associated with Vet Rec. 2003;153(4):118–121.
Pseudomonas luteola Infection. J Comp Pathol. 2012;146(1):4–10. 78. Ribeiro MG, Salerno T, Mattos-Guaraldi AL, et al. Nocardiosis: an overview
56. Mauldin EA, Peters—Kennedy J. Chapter 6—integumentary system. Jubb and additional report of 28 cases in cattle and dogs. Rev Inst Med Trop Sao
Kennedy Palmers Pathol Domest Anim 2016;1:509–736e1. Paulo. 2008;50(3):177–185.
57. McClintock DE, Banovic F, Lieske DE, et al. Pathology in practice. J Am Vet 79. Rodrigues Hoffmann A, Patterson AP, Diesel A, et al. The skin microbiome in
Med Assoc. 2021;259(S2):1–4. healthy and allergic dogs. PLoS One. 2014;9(1):e83197.
58. Milliron SM, Seyler ZG, Myers AN, et al. Pyogranulomatous panniculitis in 80. Rodrigues Hoffmann A. The cutaneous ecosystem: the roles of the skin
a domestic cat associated with Pseudomonas luteola infection. Vet Dermatol. microbiome in health and its association with inflammatory skin conditions in
2021;32(1):83-e15. humans and animals. Vet Dermatol. 2017;28(1):60–e15.
59. Montori G, Allegri A, Merigo G, et al. Intra-abdominal actinomycosis, the 81. Ross AA, Muller KM, Weese JS, et al. Comprehensive skin microbiome anal-
great mime: case report and literature review. Emerg Med Health Care. ysis revels the uniqueness of human skin and evidence for phylosymbiosis
2015;3(1):2. within the class Mammalia. PNAS. 2018;115(25):E5786–E5795.
60. Nakatsuji T, Chen TH, Narala S, et al. Antimicrobials from human skin com- 82. Sanford JA, Gallo RL. Functions of the skin microbiota in health and disease.
mensal bacteria protect against Staphylococcus aureus and are deficient in Semin Immunol. 2013;25(5):370–377.
atopic dermatitis. Sci Transl Med. 2017;9(378):eaah4680. 83. Schmidt L, Doss G, Hawkins S, et al. Cranial cervical abscessation and sial-
61. Nuttall T. Chronic pododermatitis and interdigital furunculosis in dogs. adenitis due to Pseudomonas luteola in two domestic ferrets (Mustela putorius
Companion Anim. 2019;24(4):194–200. furo). J Exot Pet Med. 2019;31:120–126.
62. O’Brien CR, Malik R, Globan M, et al. Feline leprosy due to Candidatus 84. Scott DW. Bacterial skin diseases. Color Atlas Farm Anim Dermatol. 2018:1–
“Mycobacterium lepraefelis”: further clinical and molecular characterisation 23.
of eight previously reported cases and an additional 30 cases. J Feline Med 85. Scott DW, Miller WH. Chapter 4—bacterial skin diseases. In: Equine
Surg. 2017;19(9):919–932. Dermatology. 2nd ed. Saunders; 2011:130–170.
63. O’Brien CR, Malik R, Globan M, et al. Feline leprosy due to Candidatus 86. Sears KP, Divers TJ, Neff RT, et al. A case of Borrelia-associated cutaneous
“Mycobacterium tarwinense”: further clinical and molecular characterisation pseudolymphoma in a horse. Vet Dermatol. 2012;23(2):153–156.
of 15 previously reported cases and an additional 27 cases. J Feline Med Surg. 87. Seckerdieck F, Mueller RS. Recurrent pyoderma and its underlying primary
2017;19(5):498–512. diseases: a retrospective evaluation of 157 dogs. Vet Rec. 2018;182(15):434.
64. O’Brien CR, Malik R, Globan M, et al. Feline leprosy due to Mycobacterium 88. Shimoji Y, Osaki M, Ogawa Y, et al. Wild boars: a potential source of
lepraemurium: further clinical and molecular characterisation of 23 previously Erysipelothrix rhusiopathiae infection in Japan. Microbiol Immunol.
reported cases and an additional 42 cases. J Feline Med Surg. 2017;19(7):737–746. 2019;63(11):465–468.
65. Older CE, Diesel A, Patterson AP, et al. The feline skin microbiota: 89. Smits B, Willis R, Malik R, et al. Case clusters of leproid granulomas in fox-
the bacteria inhabiting the skin of healthy and allergic cats. PLoS One. hounds in New Zealand and Australia. Vet Dermatol. 2012;23(6):465–4e88.
2017;12(6):e0178555. 90. Stacy A, Belkaid Y. Microbial guardians of skin health. Science.
66. Older CE, Rodrigues Hoffmann A, Hoover K, et al. Characterization of cuta- 2019;363(6424):227–228.
neous bacterial microbiota from superficial pyoderma forms in atopic dogs. 91. Sura R, Hinckley LS, Risatti GR, et al. Fatal necrotising fasciitis and myositis
Pathogens. 2020;9(8):638. in a cat associated with Streptococcus canis. Vet Rec. 2008;162(14):450–453.
67. Olivry T, Linder KE. Dermatoses affecting desmosomes in animals: a 92. Tham HL, Jacob ME, Bizikova P. Molecular confirmation of shampoo as the
mechanistic review of acantholytic blistering skin diseases. Vet Dermatol. putative source of Pseudomonas aeruginosa-induced postgrooming furunculo-
2009;20(5–6):313–326. sis in a dog. Vet Dermatol. 2016;27(4):320-e80.
Faccin et al 811

93. Twitchell EL, Lenz SD, Lin TL. Pathology in practice: necrotizing fasciitis, 97. Weese JS, Poma R, James F, et al. Staphylococcus pseudintermedius necrotiz-
osteomyelitis, and streptococcal septicemia in a dog. J Am Vet Med Assoc. ing fasciitis in a dog. Can Vet J. 2009;50(6):655–656.
2014;244(12):1389–1391. 98. Welle MM, Linder KE. The integument. Pathologic Basis of Veterinary
94. van Duijkeren E, Jansen MD, Flemming SC, et al. Methicillin-resistant Disease. Elsevier, 2021:1095–1262.
Staphylococcus aureus in pigs with exudative epidermitis. Emerg Infect Dis. 99. Wong JK, Chambers LC, Elsmo EJ, et al. Cellulitis caused by the Burkholderia
2007;13(9):1408–1410. cepacia complex associated with contaminated chlorhexidine 2% scrub in five
95. Wang Q, Chang BJ, Riley TV. Erysipelothrix rhusiopathiae. Vet Microbiol. domestic cats. J Vet Diagn Invest. 2018;30(5):763–769.
2010;140(3–4):405–417. 100. Woods GL, Walker DH. Detection of infection or infectious agents by use of
96. Weese J, Dick H, Willey B, et al. Suspected transmission of methicillin- cytologic and histologic stains. Clin Microbiol Rev. 1996;9(3):382–404.
resistant Staphylococcus aureus between domestic pets and humans in 101. Zinicola M, Lima F, Lima S, et al. Altered microbiomes in bovine digi-
veterinary clinics and in the household. Vet Microbiol. 2006;115(1–3): tal dermatitis lesions, and the gut as a pathogen reservoir. PLoS One.
148–155. 2015;10(3):e0120504.

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