Presenting problem: Aural Abscess in Turtles

Understanding the turtle ear

The turtle ear is a simple structure that sits caudoventral to the eye covered by a large scale called the tympanic scute (McArthur 2004, Murray 2006). As in many reptiles, the external ear is absent in chelonians. The middle ear consists of a large tympanic cavity that is bordered laterally by the tympanic membrane, which lies in direct contact with the overlying skin (Fig 1). The middle region of the skin overlying the tympanum is relatively thin so take care not to damage this area during restraint (McArthur 2004). Reptiles have only one ossicle, the columella, a long, slender bone that crosses the tympanic cavity to insert medially on the oval window of the cochlea. A narrow Eustachian tube connects the middle ear to the oropharynx (Murray 2006)

The tympanic membrane

Figure 1. The tympanic membrane sits flush against the skin underneath the tympanic scute (arrow) caudoventral to the eye. Image by Sid Mosdell. Click image to enlarge.

What is an aural abscess?

An aural abscess is a caseous plug that can slowly develop within the middle ear (de la Navarre 2000, Holladay 2001, Brown 2004, Murray 2006). Since the reptile heterophil lacks proteases capable of liquifaction, inflammatory debris appears as a firm, cheesy mass (Fig 2).

The aural abscess is a well-encapsulated, caseous plug (arrow) that fills the tympanic cavity

Figure 2. The aural abscess is a well-encapsulated, caseous plug (arrow) that fills the tympanic cavity. This ornate box turtle (Terrapene ornata ornata) actually suffered from bilateral abscessation. Image provided by Mike Comella of Wichita Falls Reptile Rescue. Click image to enlarge.

An aural abscess is composed of a necrotic center with an outer layer containing variable amounts of keratin as well as marked, diffuse inflammatory cell infiltrate. Cells frequently observed include heterophils, lymphocytes, and plasma cells (Brown 2004). Histologically the tympanic epithelium reveals squamous metaplasia, hyperplasia, and keratinization (Holladay 2001, Brown 2004). Vasculature within the lining of the tympanic cavity is moderately to markedly hyperemic (Brown 2004).

 

What causes aural abscesses?

The cause of aural abscessation is not completely understood, but affected turtles tend to have lower serum and hepatic levels of vitamin A (Holladay 2001). Hypovitaminosis A is believed to be a predisposing factor because retinoids are required for normal maintenance of healthy epithelium (Brown 2004). Vitamin A deficiency leads to squamous metaplasia and hyperkeratinization of mucin-secreting epithelium including the tympanic epithelium. When squamous metaplasia develops in the middle ear and Eustachian tube, sloughed epithelium can accumulate to form a caseous plug (Brown 2004). Secondary infection is generally associated with overgrowth of opportunistic bacteria that originate in the oropharynx and ascend the Eustachian tube (Kirchgessner 2009, Stahl 2013).

In captive turtles , vitamin A deficiency is commonly associated with poor husbandry, specifically dietary vitamin A deficiency (Brown 2004, Murray 2006, Joyner 2006). Suboptimal temperature and/or ingestion of contaminated water can also promote the development of secondary bacterial infection (Murray 2006).

The cause of aural abscessation is unknown in free-ranging turtles, however synthetic chemical environmental contaminants are believed to play a role (Joyner 2006). Increased exposure to organochlorine compounds can alter vitamin A homeostasis in birds and mammals (Poon 1995, Holladay 2001, Sleeman 2008). Reptiles may exhibit a similar sensitivity to these compounds, which can accumulate in the reptile body at levels that equal or exceed those reported in other species (Sleeman 2008). High levels of organochlorines have been associated with squamous metaplasia and aural abscessation in wild-caught box turtles (Terrapene carolina) (Holladay 2001), but it not clear that a causal relationship exists (Kroenlein 2008, Sleeman 2008).

Another potential but rare cause of hypovitaminosis A would include any condition that causes maldigestion and malabsorption as this would interfere with gastrointestinal absorption of vitamin A (Brown 2004).

 

Differential diagnoses

Clinical diagnosis of an aural abscess is usually clear-cut, however a swelling medial to the tympanic membrane can also be caused by (Kirchgessner 2009, Joyner 2006, Stahl 2013):

  • Hematoma
  • Mycobacteriosis
  • Subcutaneous parasites (protozoa, cestodes, nematodes)
  • Sebaceous cyst

Signalment

Aural abscesses are common health problems in both free-ranging and captive box turtles (Brown 2002, Brown 2003, Murray 2006, Joyner 2006, Sleeman 2008, Stahl 2013) and aquatic or semiquatic turtles, particularly red-eared sliders (Trachemys scripta elegans) (Kirchgessner 2009, Stahl 2013). In two separate surveys of free-living Eastern box turtles admitted to wildlife rehabilitation centers, aural abscess was the second most common diagnostic category seen after trauma (Brown 2002, Brown 2003, Schrader 2010).

While disease is possible in all ages, clinical problems are most commonly observed in adults. In fact the yolk sac, which is not completely resorbed until roughly 6 months of age, generally provides adequate vitamin A levels to young turtles (Kirchgessner 2009).

 

History

The chief presenting complaint for the turtle with an aural abscess is often swelling on the head. Owners of captive turtles may also report a history of anorexia (Stahl 2013).

Ask specific, but not leading, questions regarding the pet turtle’s husbandry (Murray 2006, Kirchgessner 2009):

  • What sources of vitamin A or beta-carotenoids are in the diet?
  • What is the water source?
  • What is the frequency of water changes and water bowl disinfection?

Physical examination findings

  • A semi-firm to firm mass is observed beneath the tympanum (Murray 2006).
  • The swelling can appear slightly yellow due to the caseous material within the tympanic cavity (Murray 2006).
  • The swelling can be unilateral or bilateral and can vary dramatically in size (Brown 2003, Murray 2006, Joyner 2006).
  • A head tilt is sometimes observed (Stahl 2013), presumably due to pain.
  • Take care when palpating the swelling as pressure can express debris through the Eustachian tube into the oropharynx (Murray 2006, Kirchgessner 2009).
  • Concurrent findings caused by hypovitaminosis A, but unrelated to aural abscessation, can also be observed.

Potential signs of hypovitaminosis A that can be observed in chelonians in addition to aural abscessation (Kirchgessner 2009)

  • Blepharedema, blepharospasm
  • Conjunctivitis
  • Blindness (evidence of)
  • Rhinitis
  • Lower respiratory tract disease (manifesting as nasal discharge, depression, dyspnea)
  • Abnormally thick or thin skin, skin sloughing or blistering

Key points of urgent care

Many turtles that present with an aural abscess are debilitated and will benefit from a delay in surgical intervention (de la Navarre 2000, Murray 2006, Kirchgessner 2009, Stahl 2013):

  • Warm the patient to the upper end of its preferred optimum temperature zone.
  • Correct fluid and electrolyte imbalances.
  • Provide nutritional support.
  • Begin systemic, broad-spectrum antibiotics in patients with evidence of systemic illness based on physical examination and hematologic findings (Murray 2006).
  • Provide analgesia such as butorphanol (0.4-1.0 mg/kg SC, IM) (Schumacher 1996). Make sure the patient is well hydrated before instituting anti-inflammatory therapy like meloxicam (0.5 mg/kg PO, IM) (Rojos-Solís 2009).
  • A single injection of vitamin A may also be deemed appropriate in select cases (see below).

Supportive care may decrease the local inflammatory response, which in turn can reduce intraoperative bleeding. Schedule surgery (see below) when the turtle’s mentation, attitude, and hydration status have improved (de la Navarre 2000).

 

Diagnosis

Clinical diagnosis is based on observation of a swelling medial to the tympanic membrane and confirmed by surgical exposure of caseous material within the ear (Brown 2003, Joyner 2006, Kirchgessner 2009). Additional tests are sometimes indicated to determine the best treatment plan as well as the prognosis (Murray 2006):

    • Aerobic/anaerobic culture and sensitivity testing

Culture is a valuable diagnostic tool because there is no one bacterial agent that is responsible for aural abscess in turtles. Aerobic Gram-negative bacteria are most commonly implicated, however these organism tend to have unpredictable antibiotic susceptibilities. Gram-positive bacteria and anaerobes have also been reported in aural abscesses (Brown 2004, Joyner 2006).

Bacterial agents reported in turtle aural abscesses (Joyner 2006, Murray 2006, Stahl 2013)

      • Aeromonas
      • Citrobacter
      • Escherichia
      • Klebsiella
      • Morganella*
      • Proteus
      • Providencia
      • Pseudomonas
      • Salmonella
      • Corynebacteria
      • Staphylococcus epidermidis
      • Streptococcus spp.
      • Bacteroides
      • Clostridium
      • Fusobacterium

*In a study evaluating free-ranging Eastern box turtles (Terrapene carolina) with aural abscesses, only Morganella morganii was isolated from the tympanic cavity of multiple turtles (Joyner 2006).

Although Mycoplasma agassizii has been associated with respiratory tract disease in chelonians, no correlation has been identified between the presence of Mycoplasma sp. in free-ranging Eastern box turtles and aural abscesses (Feldman 2004, Joyner 2006).

Needle aspiration is typically non-diagnostic, therefore culture samples should be collected intraoperatively (Murray 2006, Stahl 2013).

    • Cytology

Culture results are sometimes negative, so use cytology to gain some idea of the bacteria involved and to screen the patient for unusual etiologic agents like Mycobacterium spp. Like culture samples, cytologic specimens should be collected surgically and not by fine needle aspiration (Murray 2006, Stahl 2013). Potential staining techniques to perform include Romanowski (e.g. Diff-Quick) and acid-fast staining, direct smears, and/or impression smears (Stahl 2013).

    • Blood work

The complete blood count can sometimes be used to find evidence of systemic illness such as leukocytosis, monocytosis, azurophilia, and/or toxic shift (Murray 2006, Stahl 2013). Use caution when interpreting lab results, as hematologic values in reptiles can be affected by a host of factors including age, gender, environment, season, and nutritional status (Campbell 2006, Schrader 2010).

Vitamin A deficiency can lead to hepatic lipidosis, and a biochemistry panel can sometimes detect related organ involvement (Campbell 2006, Kirchgessner 2009).

    • Imaging

Bony infection can adversely affect prognosis. Use survey radiographs to look for evidence of osteomyelitis involving bones adjacent to the middle ear, like the quadrate bone. Imaging is also occasionally used to differentiate inflammation from neoplasia (McKlveen 2000, McArthur 2004, Stahl 2013).

    • Histopathology

Submit a biopsy sample for histologic evaluation when a diagnosis of aural abscess is in question.

 

Therapy

    • Client education

While the pet turtle is hospitalized, the owners should take measures to improve any deficiencies in husbandry including the temperature gradient, water sanitation practices, and nutrition. Beta-carotenoid-rich foods should be offered such as orange and yellow vegetables or dark, leafy greens (Murray 2006, Stahl 2013). Some clinicians recommend feeding a small amount of chicken liver once weekly to aquatic turtles (Kirchgessner 2009), however there is a risk of exposure to Salmonella spp. that are potentially pathogenic to turtles (van Duijkeren 2002).

    • Surgical management

Treatment of an aural abscess requires surgical removal of the entire, well-encapsulated mass under general or local anesthesia (Kirchgessner 2009, Stahl 2013). Some clinicians prefer propofol (10 mg/kg slow bolus IV) because the procedure is relatively short (de Navarre 2000, Murray 2006). Medetomidine-ketamine is another popular combination. A regimen recommended in red-eared sliders is medetomidine (0.2 mg/kg IM) with ketamine (10 mg/kg IM), reversed with atipamizole (1.0 mg/kg IM) (Greer 2001).

Intubate the turtle whenever possible to minimize the risk of aspiration (Kirchgessner 2009). If for some reason intubation is not possible, check the oropharyngeal cavity frequently for evidence of caseous debris (Murray 2006). Perform a sterile surgical preparation of the area, particularly when a culture sample will be collected (de la Navarre 2000, Murray 2006). Take care to protect the eyes during preparation of the surgical site (McArthur 2004).

A variety of surgical approaches have been described, however a popular technique involves the creation of a full-thickness, horizontal incision through the tympanum from 9 o’clock to 3 o’clock. Extend the incision along the ventral border of the ear to create a C-shaped opening. Carefully remove debris using small ear loops, curettes, or forceps while avoiding the columella (de la Navarre 2000, Murray 2006). Completely remove all caseous material, preferably in one large piece, although not all abscess are encapsulated (Fig 3) (de la Navarre 2000, McArthur 2004). Hemorrhage is generally limited and easily controlled with pressure or light cautery (McArthur 2004).When done, carefully examine the entire region since debris can extend quite far even into the caudal-most regions of the tympanic cavity (de la Navarre 2000).

Remove the entire caseous plug whenever possible

Figure 3. Remove the entire caseous plug in toto (arrow) whenever possible. Image by Mike Comella of Wichita Falls Reptile Rescue. Click image to enlarge.

Collect samples for culture and cytology, then flush the tympanic cavity with copious amounts of warm, dilute antiseptic solution (e.g. 1 part chlorhexidine to 30 parts sterile water) (Murray 2006, Kirchgessner 2009, Stahl 2013). While flushing, direct the turtle’s head so that the nares are ventral to the ears so that any debris and fluid that enters the oropharynx will exit the mouth (de la Navarre 2000). Also in the intubated turtle, pass a small irrigating cannula and flush the Eustachian tube with saline. Place a moistened gauze or a swab in the caudal pharynx to reduce the risk of aspiration (McArthur 2004).

After lavage, pack the wound with an antibiotic ointment like gentamicin ophthalmic ointment or silver sulfadiazine cream (Silvadene, Monarch Pharmaceuticals) (Murray 2006). Continue local wound treatment for approximately 1 week post-operatively before allowing the wound to close by second intention (de la Navarre 2000, Murray 2006, Stahl 2013).

    • Medical management

Systemic antibiotics are often indicated; adjust therapy based on sensitivity results (Kirchgessner 2009, Stahl 2013). Continue analgesia and/or anti-inflammatory therapy as needed.

Resist the urge to inject all turtles suffering from aural abscessation with vitamin A as hypervitaminosis can occur with even one parenteral injection. Cautiously use injectable vitamin A only in select cases, such as patients with severe disease and/or secondary ocular problems caused by vitamin A deficiency. Select an oil-based injectable supplement and give a single injection (1000-2000 IU/kg IM) followed by oral supplementation and dietary sources of beta-carotene (Kirchgessner 2009). If the patient must be tube fed, add an oral supplement to the formula.

Small patient size means that injectable vitamin A must often be diluted. Whenever possible, use a compounding pharmacist to create a safe and accurate dilution. If dilutions are created in-house, use propylene glycol instead of saline or sterile water since vitamin A is fat-soluble (Kirchgessner 2009).

 

Follow-up

To ensure that infection has cleared, recheck patients approximately 5-7 days post-operatively before the surgical site seals over (Fig 4). If active osteomyelitis has been identified, more frequent evaluations using survey radiographs may be indicated to assess patient progress (Stahl 2013).

 Re-evaluate the turtle before the stoma heals over completely

Figure 4. Reevaluate the turtle before the stoma (arrow) heals over completely. Image by Mike Comella of Wichita Falls Reptile Rescue. Click image to enlarge.

Prognosis

Most turtles with aural abscesses respond well to surgical treatment and heal completely (de la Navarre 2000, Schrader 2010). Depending on the severity of disease, all clinical signs related to hypovitaminosis A generally resolve within 2 to 6 weeks (de la Navarre 2000).

Disease can recur when vitamin A deficiency is not addressed, the granuloma is not completely removed, or when bony infection is present. In fact patients with underlying osteomyelitis tend to suffer from a more guarded or even poor prognosis (de la Navarre 2000, Murray 2006, Stahl 2013).

It is unclear how hearing is affected by the granuloma and surgical debridement, however chelonians do not appear to suffer any long-term adverse effects (de la Navarre 2000, Murray 2006). Chelonians are only capable of hearing low tones and the ears may be more important for balance (McArthur 2004).

References