Presenting problem: Stomatitis in Reptiles

Key Points

  • Stomatitis is a common problem in snakes and lizards; disease is less common in chelonians.
  • Affected squamates can exhibit a variety of clinical signs including anorexia, dulled mentation, red, inflamed and swollen gingiva, mucus or discharge from the mouth, and open-mouth breathing.
  • An important differential diagnosis is primary respiratory disease as these patients can also present with thick oral mucus and hyperemia of the gingiva.
  • Multiple factors can contribute to stomatitis in squamates, however primary or secondary Gram-negative bacterial infection is an important component of disease.
  • Irrigate inflamed tissues regularly with an antiseptic solution.
  • Ensure the patient is maintained at its preferred optimum temperature zone.
  • Long-term systemic antibiotics are indicated for patients with cellulitis.
  • Testudinid herpesvirus causes a stomatitis-rhinitis complex in tortoises, particularly Mediterranean tortoises (Testudo spp).
  • Hypovitaminosis A is an important cause of stomatitis in box turtles and aquatic tortoises.
  • When left untreated, stomatitis can progress to osteomyelitis, panophthalmitis, dacrocystitis, pneumonia, and/or death.

Understanding stomatitis

Incidence of stomatitis

Stomatitis, also known as “mouth rot”, ulcerative stomatitis, necrotic stomatitis, and/or periodontal disease is a common problem in snakes and lizards (Diaz-Figueroa 2006) (Fig. 1). Stomatitis is less common in chelonians and crocodilians, and often presents as a stomatitis-rhinitis complex in tortoises.

Stomatitis in a red-tailed boa

Figure 1. Stomatitis in a red-tailed boa (Boa constrictor imperator). Image by Dr. Shane Simpson. Click image to enlarge.

Pertinent anatomy

There is tremendous diversity in Class Reptilia and tooth morphology ranges over a continuum that rarely fits into one simple category (Kardong 2011). All snakes and many lizards possess pleurodont dentition. There are no teeth sockets, and each tooth is attached to bony ridges on the medial surface of the jawbones. In some species with pleurodont dentition, the teeth are regularly shed and replaced throughout life (Wyneken 2011, Barten 2006).

Family Agamidae, such as water dragons and bearded dragons, Chamaeleonidae, and Sphenodontidae (tuataras) are important exceptions to this rule of thumb. Except when young and growing, these lizards do NOT replace their teeth and they are at significant risk for periodontal disease (Barten 2006, Nevarez 2009). This type of dentition is often referred to as “acrodont” in reptile literature—although experts in the field of tooth diversity and development are increasingly abandoning this term (Jeanette Wyneken, personal communication 2013).

 

Key points of urgent care

Stomatitis is often a chronic, insidious condition and the majority of cases that present on an emergency basis do not require urgent care.

Refer to case management (below) for recommendations on care of mild cases. More severely affected animals require aggressive supportive care such as supplemental heat and fluid therapy.

 

Case management of squamates

Signalment

  • Among snakes, stomatitis is particularly common in boa constrictors (Boa constrictor), reticulated pythons (Python molurus bivitattus), and Burmese pythons (Python reticulatus) (Stahl 2013).
  • Lizards with acrodont dentition, such as water dragons and bearded dragons, are also at increased risk for stomatitis. The teeth are not rooted but simply attached to jaw bones creating more exposure of gingiva and increasing the risk of bacterial invasion (Stahl 2013, McCraken 1994) (Fig 2).

    Stomatitis in a central bearded dragon

    Figure 2. Stomatitis in a central bearded dragon (Pogona vitticeps) with acrodont dentition. Image by Dr. Shane Simpson. Click image to enlarge.

  • Glands at the commissures of the mouth may also be prone to abscessation in Old World chameleons (Stahl 2013).

History

Obtain a complete history that includes medical information as well as detailed husbandry information.

  • What is the presenting complaint?Owners of reptiles with stomatitis often report non-specific signs of illness such as lethargy and anorexia. Dysphagia and ptyalism may also be observed.
  • What is the housing set-up?Reptiles suffer from increased susceptibility to infection when they are not housed at an appropriate temperature gradient.Poor cage design and lack of cage furniture can increase the risk of traumatic lesions (see pathogenesis below).
  • What is the animal fed and what proportions of the diet does the reptile actually eat?Hypovitaminosis A can be a risk factor in the development of stomatitis.

Visual examination

Careful observation of the reptile with stomatitis may reveal drooling and/or open-mouth breathing. The mouth may not close symmetrically.

Physical examination

Perform a complete physical exam (Box 1), using extreme caution when opening the mouth to minimize the risk of further trauma (Fig 3). The mouths of many squamates can be opened by gently pulling down on the skin beneath the jaw (Fig 4). If a mouth speculum is necessary, beware that use of tongue depressors, hemostats, or other rigid instruments can aggravate the problem. Use of a folded piece of radiographic film or a rubber spatula allows for gentle manipulation of the mouth.

Box 1. Physical exam findings commonly seen in snakes and lizards with stomatitis

  • Red, inflamed gingiva

  • Blood, mucus, or purulent discharge within or coming from the mouth

  • Petechial or ecchymotic hemorrhages

  • Pockets of caseous debris and abscessation

  • Teeth loss

  • Swelling of the perioral region or head

  • Asymmetry to closure of the mouth

Use caution when opening the mouth to minimize the risk of further trauma.

Figure 3. Use caution when opening the mouth to minimize the risk of further trauma. Image by Edward Ramsay. Click image to enlarge.

Gently pulling down on the dewlap of an iguana to open the mouth

Figure 4. Shown here, gently pulling down on the dewlap of an iguana to open the mouth. Click image to enlarge.

Physical examinations findings commonly range from redness and discharge to swelling and tooth loss (Box 1) (Fig 5). Stomatitis can also sometimes progress to tongue sheath abscesses, and even tongue paralysis, in chameleons, monitors and snakes (Mehler 2006).

Severe stomatitis lesions in a lizard.

Figure 5. Severe stomatitis lesions in a lizard. Image provided by Dr. Tom Tully. Click image to enlarge.

Pathogenesis

Infectious stomatitis is often a multifactorial disease process in which bacterial infection arises secondary to underlying trauma and/or poor husbandry conditions.

  • Stress from improper temperature or humidity, poor diet, and/or crowding can lead to immunosuppression.
  • Trauma allows bacterial invasion. Males can abrade their snout or “lip” margins during repeated attempts to escape their cage during the breeding season. High-strung or nervous squamates without appropriate visual security can also traumatize themselves by repeatedly striking at any movement that occurs near the cage. A difficult shed, or dysecdysis along the “lip” margins can also allow bacterial invasion.
  • Vitamin A deficiency is thought to play an important role in the development of stomatitis in Old World chameleons, anoles, and fat-tailed geckos (Hemitheconyx caudicinctus). Reproductively active females and juvenile lizards also have relatively high needs for dietary vitamin A (Stahl 2013).

Stomatitis in squamates is typically caused by opportunistic Gram-negative bacterial infection (Box 2). Anaerobic bacteria, such as Clostridium, Eubacterium, Anaerobiospirillum, frequently complicate infection and Gram-positive organisms can also be isolated from oral lesions. There are even rare reports of tuberculous stomatitis in boa constrictors (Olson 1987, Quesenberry 1986).

Box 2. Numerous Gram-negative bacteria can be associated with stomatitis in reptiles

  • Aeromonas spp.

  • Pseudomonas spp.

  • Citrobacter spp.

  • Alcaligenes spp.

  • Citrobacter spp.


  • E.coli

  • Klebsiella spp.

  • Pasteurella spp.

  • Proteus spp.

  • Salmonella spp.

Particularly common organism are bolded

There are conflicting reports on the incidence of fungal stomatitis (Cheatwood 2003), and some authors believe this condition may be under-reported (Mehler 2006).

Differential diagnoses

  • Respiratory tract diseaseSome primary respiratory problems can present with thick oral mucus and hyperemia of the gingiva. Stomatitis can also develop secondary to chronic open mouth breathing with underlying respiratory infection
  • Neoplasia
  • Nutritional secondary hyperparathyroidism (metabolic bone disease)
  • Dehydration
  • Visceral goutRenal failure and other conditions associated with marked hyperuricemia can lead to visceral gout including diffuse, white plaques or nodules on gingival mucosa (Mehler 2006).

Diagnostics

Preliminary data should ideally include:

  • Complete blood countTypical findings can include leukocytosis and heterophilia. Monocytosis, azurophilia, and toxic changes may be seen with severe disease. Anemia is a frequent finding in chronic cases (Diaz-Figueroa 2006, Johnson 1996).
  • Cytology, bacterial culture and sensitivity of the deeper pockets of infectionUse caution when interpreting culture results, as many of the microorganisms isolated are opportunistic, environmental microbes (Klarsfeld 2002).
  • Survey radiographs to evaluate the patient for underlying bony lesions.

Biochemistry panel and fecal parasite testing (direct saline smear and fecal flotation) are standard components of the minimum database, however results are not typically affected by stomatitis.

  • Fecal parasite testing is routinely performed in all sick reptiles, and heavy parasitism is an important cause of immunosuppression.
  • A biochemistry panel is generally performed in stomatitis cases only to rule-out other differential diagnoses.

Therapeutics

Consider referral of advanced cases or those involving lizards with acrodont dentition as recurrent, chronic treatment is often required.

    1. Correct husbandryEducate the owner on husbandry practices that require improvement or correction. Visit LafeberVet’s Basic Information Sheets for housing recommendations of select reptile species.
    2. Debridement and lavageProvide intense local therapy to inflamed tissues. Gently debride gingiva as needed (Fig 6), and irrigate tissues daily with an antiseptic solution (Box 3). Many clinicians prefer 0.05% chlorhexidine solution because it can be effective against Pseudomonas spp., however 1% iodine solution can also be used. Avoid allowing the patient to ingest the antiseptic solution as this can cause gastrointestinal disturbance, particularly in herbivorous reptiles.
      Box 3. Safety tip
      Wear exam gloves and eye protection (goggles) when treating reptiles with infectious stomatitis to minimize your exposure to the heavy load of pathogenic flora
      In many advanced cases, surgical debridement of necrotic bone is necessary.
Stomatitis, pre- and post-debridement

Figure 6. Stomatitis, pre- (left) and post-debridement (right) in a coastal carpet python (Morelia spilota mcdowelli). Image by Dr. Shane Simpson. Click image to enlarge

  1. Antimicrobial therapyUncomplicated cases of stomatitis that are recognized early can be managed with topical treatment alone. Apply silver sulfadiazine cream (Silvadene, Monarch Pharmaceuticals) to oral lesions. This gentle, water-soluble cream is often effective against Pseudomonas spp. As with chlorhexidine solution, be sure to minimize ingestion.For patients with moderate to severe stomatitis evidenced by cellulitis, long-term systemic antibiotics are indicated (minimum 2 weeks). Gram-negative bacteria possess unpredictable susceptibilities and antimicrobial therapy should ideally be based on the results of culture/sensitivity testing. While lab results are pending, popular empirical choices include piperacillin (100 mg/kg q48-72h), enrofloxacin (5-10 mg/kg IM q24-48h short-term), aminoglycosides (amikacin 5 mg/kg IM, then 2.5 mg/kg q72h), ceftazidime (20 mg/kg SC, IM q72h), and carbenicillin (Gibbons 2013, Mader 1985, Lawrence 1984). Include fluid therapy when administering aminoglycosides.
  2. Supportive careMaintain hydration with fluid therapy. Suedmeyer recommends Tyrode’s solution, an easily obtained fluid that approaches physiologic saline for reptiles.
  3. Vitamin A therapySupplemental vitamin A may aid in healing of some lizards like chameleons (Stahl 2013). Oil-based formulations can be a better choice for acute treatment (1000-2000 U/kg), and absorption from oral dosing may be safer in preventing vitamin A toxicity (2000 U/30 g PO) (Gibbons 2013, Stahl 2013).

Case management of chelonians

With the exception of Testudinid herpesvirus, management of stomatitis in turtles and tortoises is very similar to that in snakes and lizards. Therefore the following section focuses on management of herpesvirus in chelonians while also touching on management of vitamin A deficiency in turtles.

Signalment

  • Aquatic turtles and box turtles are particularly susceptible to vitamin A deficiency and subsequent stomatitis.
  • All tortoise species can develop stomatitis-rhinitis complex caused by Testudinid herpesvirus, also known as chelonian herpesvirus (ChHV) infection (Jacobson 2012). Mediterranean tortoises appear to be most susceptible to Testudinid herpesvirus (Marschang 2009, Hunt 2006). Herpesviral infections are most commonly seen during seasonal changes, particularly the spring (Wellehan 2013, Origgi 2006).

History

Obtain a complete history that includes medical information as well as detailed husbandry information.

  • What is the presenting complaint?Owners often report non-specific signs of illness such as lethargy and anorexia. Oculonasal discharge may also be reported with herpesviral infection. Visual deficits can be detected with hypovitaminosis A.
  • Have any new tortoises been introduced? What sanitation and quarantine practices are used?Testudinid herpesvirus is spread by direct contact. Like most herpesviruses, the organism does not persist long in the environment and is susceptible to dilute sodium hypochlorite (Wellehan 2013).
  • Are any other reptiles owned? Are the reptiles housed together or singly?Aquatic turtles appear to be particularly sensitive to suboptimal husbandry conditions.
  • Are there any changes in the environment?Stressors can increases the likelihood of a latent herpesvirus infection becoming clinical (Wellehan 2013).
  • Describe the housing set-up.
  • What is the animal fed and what proportions of the diet does the reptile actually eat?Hypovitaminosis A can be a risk factor in the development of stomatitis, particularly in aquatic turtles and box turtles.

Visual examination

Careful observation of the patient may reveal:

  • Signs of lethargy such as reluctance to come out of the shell, inactivity, and/or absence of truncal lift.
  • Oculonasal discharge is frequently seen with stomatitis caused by Testudinid herpesvirus. Oral discharge can also be observed and may manifest as a dry, white deposit along the lower beak (Origgi 2006).

Physical examination

Perform a complete physical exam (Box 4), using extreme caution when opening the mouth. Many chelonian mouths can be opened by pressing down on the lateral sides of the beak. Rubber spatulas, baby spoons, or well-padded hemostats allow gentle manipulation of the mouth.

Box 4. Physical exam findings commonly seen with Testudinid herpesvirus

  • Diphtheritic, often yellow fibrous, oral plaques

  • Glossitis or inflammation of the tongue

  • Serous to mucopurulent nasal discharge, sometimes obstructing nares

  • Serous to mucoid ocular discharge

  • Swollen eyelids or blepharedema

Physical exam findings commonly seen with Testudinid herpesvirus include oropharyngeal plaques and oculonasal discharge (Box 4). Waxing and waning unilateral or bilateral ocular lesions can also be seen in chelonians with Testudinid herpesvirus stomatitis-rhinitis complex. With advanced or chronic herpes, tortoises can also exhibit dyspnea, cachexia. In rare instances, neurologic signs, such as circling and head tilt are observed.

Differential diagnoses

Testudinid herpesvirus and hypovitaminosis A are important causes of stomatitis in turtles and tortoises (Box 5).

  • Herpesvirus particles or herpesvirus-like particles have been identified in epidemics or outbreaks associated with stomatitis-rhinitis in tortoises (Origgi 2006).
  • As in some lizard species, hypovitaminosis A can be a risk factor in the development of stomatitis, particularly in aquatic turtles and box turtles.
Box 5. Potential causes of stomatitis in chelonians
D
A
MMetabolicVisceral gout
NNeoplasia
Nutritional
Hypovitaminosis A
IInfection
Inflammation
Chelonian herpesvirus
Iridovirus
Ranavirus (Johnson 2008)
Chlamydophila (Soldati 2004, Hotzel 2005)
TTrauma
Differentials or factors that play a major role in chelonian stomatitis are bolded.

Note: Mycoplasma spp. does not cause stomatitis, but instead causes upper and lower respiratory respiratory infections. Consider mycoplasmosis as part of due diligence in addressing sequella to stomatitis.

Diagnostics

  • Obtain a minimum database as described in squamates.There is one case report in spur-thighed tortoises (Testudo graeca) that describes clinical pathologic findings with herpesvirus (Box 6) (Muro 1998).
    Box 6. Blood test results in spur-thighed tortoises (Testudo graeca) with chelonian herpesvirus

    • Lymphocytosis

    • Heteropenia

    • Elevated aspartate aminotransferase

    • Elevated alpha-globlulins

    • Normocytic-normochromic anemia

  • SerologySerologic testing, such as ELISA, is used to screen the patient for exposure to herpesvirus. Serology is considered the diagnostic test of choice during chronic or latent stages of disease, however some available tests are serotype-specific, so use caution when interpreting results.
  • PCR testingPolymerase chain reaction testing in tortoises for Testudinid herpesvirus is most useful during the acute phase of disease (Origgi 2006). Submit swabs or biopsies of fresh mucocutaneous lesions (Box 7).
    Box 7. Laboratories with available chelonian herpesvirus testing
    InstitutionSerologyPCR TestSubmission forms or contact information
    Hohenheim UniversityXXContact Rachel Marschang at rachel.marschang@googlemail.com
    Royal Veterinary CollegeXhttp://www.rvc.ac.uk/DLS/Services.cfm
    University of BernELISAXContact Dr. Francisco Origgi at
    francesco.origgi@vetsuisse.unibe.ch
    University of FloridaXhttp://labs.vetmed.ufl.edu/sample-requirements/microbiology-parasitology-serology/zoo-med-infections/
  • Viral isolation is needed for definitive diagnosis of viral infection, however specialized tools and personnel are required.
  • Perform bacterial culture/sensitivity testing as needed.

Therapeutics

Management of chelonian stomatitis will vary with the underlying cause. Chelonian herpesvirus cases can be difficult to manage; consider referral to an experienced reptile veterinarian.

  1. Educate the owner on husbandry practices that require improvement or correctionVisit LafeberVet’s Basic Information Sheets for housing recommendations of select species.
  2. Supportive careAggressive efforts to stabilize the patient often rely upon fluid therapy and nutritional support.
  3. Supplemental vitamin ASupplemental vitamin A can be indicated to maintain epithelial integrity and aid in healing in box turtles and aquatic turtles (Box 8).
    Box 8. Recommended acute vitamin A dosing in chelonians (Stahl 2013)
    Type of chelonian
    Dose
    Aquatic turtles200-300 IU/kg SC, IM
    Box turtle1000-2000 IU/kg SC, IM
  4. Antiviral therapyAntiviral therapy is generally reserved for tortoises with confirmed herpesviral infection. Antiviral agents, ganciclovir and acyclovir, have been found to inhibit replication of Testudinid herpesvirus in vitro (Marschang 1997). Anecdotal reports have recommended acyclovir (80 mg/kg PO q24h) in clinically ill tortoises (Gopherus agassizii) (Origgi 2006), although poor oral absorption has been documented at this dose (Gaio 2007).
  5. Antimicrobial therapySystemic injectable antibiotics are indicated in severe cases of stomatitis to cover secondary bacterial infections or when concurrent Mycoplasma agassizii infection is suspected (Salinas 2011, Soares 2004). Popular empirical choices include macrolides (clarithromycin 15 mg/kg PO q 48-72h) and tetracyclines (doxycycline 50 mg/kg IM, then 25 mg/kg q 72h) (Wimsatt 1999, Spörle 1991). Avoid fluoroquinolones, as enrofloxacin treatment is likely to result in a Mycoplasma carrier state that can recrudesce later (Wellehan 2013).
  6. Consider “herd health”Herpesviruses are relatively unstable in the environment and transmission typically relies upon direct contact between animals. Testudinid herpesvirus can persist in the soil for months (Wellehan 2013, Marschang 2005).
    • Separate sick tortoises from healthy tortoises
    • Replace contaminated soil (or turn over and expose soil to sunlight)
    • Disinfect the facility using dilute 3% sodium hypochlorite
    • Discard contaminated fomites that cannot be sanitized
    • Educate the owner on basic quarantine principles such as feeding and treating ill chelonians last and washing hands after handling

Prognosis

Stomatitis is a potentially serious condition, that when left untreated can spread to include the jaw bones, eyes, nasolacrimal duct, and/or respiratory tract.

  • Fortunately with treatment, simple cases of stomatitis in reptiles typically resolve within 10 to 14 days.
  • Complicated cases require weeks or even months to resolve, and recurrence is common when osteomyelitis or abscessation are present. Recurrence is also much more likely when Pseudomonas spp. is isolated, as this microbe tends to be particularly resistant to antimicrobial therapy (Stahl 2013).
  • Prognosis with herpesviral infection varies with a number of factors including viral dose. High viral load translates to a worse prognosis. Systemic lesions involving the liver and spleen are commonly observed in severely affected chelonians (Hervás 2002).

Summary

Stomatitis is a common problem in squamates. The condition is less common in chelonians. The clinical picture can include non-specific signs of illness such as a reduced appetite and lethargy, red and swollen gingiva, mucoid or exudative discharge from the mouth, and even respiratory difficulty. The underlying cause of stomatitis is believed to be multifactorial with trauma and stress secondary to overcrowding or poor husbandry being particularly important. The etiologic agent is often Gram-negative bacteria. Testudinid herpesvirus can cause stomatitis-rhinitis complex in tortoises. Stomatitis is generally a chronic, insidious condition that rarely requires urgent care measures, however aggressive supportive care is indicated. Although topical management is adequate for mild or early cases, moderate to severe disease calls for systemic antibiotic therapy.

References