Ethical statement

Rehabilitation of sea turtles at the New England Aquarium during the years included in this study was authorized by the US Fish and Wildlife Service by Permits TE-697823 and ES69328D and at the National Aquarium by Permit TE-70312D.

Case selection criteria

Clinicians at sea turtle rehabilitation facilities along the eastern coast of the US were emailed in 2023 regarding cases of trismus in sea turtles previously in their care. Responses were received from veterinarians at the New England Aquarium, National Aquarium, North Carolina Aquariums, Karen Beasley Sea Turtle Rescue and Rehabilitation Center, South Carolina Aquarium, Georgia Sea Turtle Center, and The Turtle Hospital. Six cases of trismus were identified via memory of individual clinicians and medical database searches, with 3 facilities having no recorded cases and 1 facility having several cases in clinician memory but no longer having access to medical records (records were destroyed by a hurricane). Inclusion criteria for the present study included clinical evidence of trismus or signs of jaw pain and advanced diagnostic imaging (CT or MRI) or histopathologic evidence of disease in the head or neck. These criteria limited cases to those from the New England Aquarium and the National Aquarium, all of which were initially stranded due to cold-stunning. All included cases occurred between 2009 and 2023 and are presented in chronological order.

Consistent with established practices and common disease conditions, cold-stunned turtles were gradually warmed and reintroduced to water; assessed through physical examination, clinical pathologic analyses, and serial radiographs; and treated with parenteral fluid therapy, antibiotics, and nutritional support as needed.²¹ Additional individual treatment plans were established based on cumulative clinical data. Herein we provide detailed descriptions as relevant to trismus diagnosis and management and only brief descriptions regarding important comorbidities and their management. Details of parenteral fluid therapy often vary daily based on physiologic status and are thus only summarized. The number of blood samples obtained by jugular venipuncture before the evaluation of trismus was recorded for each case to consider the potential for iatrogenic causes of cervical tissue injury. Treatment durations and intervals were determined relative to the date of initial rescue.

Case 1

A 2.5-kg juvenile cold-stunned Kemp's ridley sea turtle was evaluated on day 48 of rehabilitation when staff noted that the animal had started to show interest in voluntary feeding but appeared reluctant or unable to open its mouth. The animal had been evaluated previously on day 12 of rehabilitation due to weakness and resting at the surface and was diagnosed with severe pneumonia via radiographs and tracheal lavage and treated with antimicrobials (Supplementary Table S1). Blood culture was negative. Due to poor body condition and anorexia, tube feeding was initiated every other day (10 mL/kg herring filet gruel, 25 mg/kg calcium carbonate, and Sea Tab B.T.F.S. multivitamin one-fourth tablet, days 11 to 47). For tube feeding, the mouth was opened manually by clinicians, a modified Nylabone (Central Garden & Pet Company) was used as a speculum to keep the mouth open, and a 14-French red-rubber catheter was passed to the distal esophagus or stomach. At the time of evaluation for trismus, hematologic and plasma biochemical analysis revealed a severely elevated creatine kinase (CK; 93,141 U/L), AST (1,337 U/L), LDH (> 36,000 U/L), and mild hypoproteinemia (total protein, 2.7 g/dL). Physical examination detected an apparent pain response characterized by muscle tremors of the flippers and withdrawal of the head during palpation of the caudal mandibular region. Skull and cervical radiographs were unremarkable. Seventeen jugular venipuncture procedures had been performed before trismus presentation. The condition was suspected to be caused or exacerbated by restraint of the jaw, so tube feedings and oral medications were discontinued and meloxicam (0.4 mg/kg, IM, q 24 h) was prescribed. Eight days later, the turtle remained interested in food but was unable to open its mouth wide enough to consume sufficient food mass. The turtle was anesthetized for oral evaluation, during which clinicians noted difficulty opening the mouth > 3 cm. The anesthesia doses were ketamine 5 mg/kg IV and medetomidine 0.05 mg/kg IV. Vitamin E/selenium (0.065 mg/kg selenium, 3.25 mg/kg vitamin E, IM, once weekly) and daily subcutaneous fluids (1 part lactated Ringer solution: 2 parts 2.5% dextrose and 0.45% saline; 10 mL/kg, q 24 h, days 49 to 76) were prescribed, and a single dose of methylprednisolone sodium succinate (0.8 mg/kg per site, 1.6 mg/kg total) was injected into the region of each jaw joint. True intraarticular injection could not be confirmed. Meloxicam was discontinued. Computed tomography and MRI were performed 2 days later and interpreted by a board-certified veterinary radiologist (JOB), using gadopentetate dimeglumine contrast (100 mg/kg, IV) for MRI. Computed tomography did not reveal an obvious cause for the observed clinical signs. Magnetic resonance imaging findings were consistent with right temporal and dorsal cervical muscle myositis, including marked inhomogeneous T2 hyperintensity of the temporalis muscle and right dorsal aspect of the neck to the level of the third cervical vertebra with marked inhomogenous enhancement (Figure 1). The next day, acupuncture treatment was initiated by a Licensed Acupuncturist (CAM) and was continued weekly for a total of six 15- to 20-minute treatments. Acupuncture channels with fascial connections to the lateral head and jaw were activated using sterile 40-gauge filiform needles inserted less than 5 mm deep. Acupuncture points were located on the head, latissimus dorsi, between the radius and ulna, at the head of the fibula, and on the extremities of the limbs. Each treatment included extrapolated meridian points from the following list: LI4, TW5, GB21, ST4, GV20, GB32, GB34, ST 36, ST44, and LV3.

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Precontrast T2-weighted MRI axial (A) and coronal (B) images of asymmetrical inhomogenous hyperintensity of the right temporal and dorsal cervical musculature (white arrows) consistent with myositis in a Kemp's ridley sea turtle (Lepidochelys kempii, case 1). Contrast enhancing T1-weighted MRI axial (C) and coronal (D) views of asymmetrical homogenous hyperintensity of the left temporal and dorsal cervical musculature (white arrows) consistent with myositis in a loggerhead sea turtle (Caretta caretta, case 3). Noncontrast CT images of asymmetrical inhomogenous hyperattenuating cervical musculature (white arrows) in a Kemp's ridley sea turtle (case 5). The 3-D volume renderings (E from a dorsal view and G from a left-sided view) represent the plane of the adjacent 2-D slices (F and H), indicated by a white reference line. Images F and H are displayed in a soft tissue window (window width, 33 HU; window level, 190 HU; 1-mm slice thickness). C3 = Third cervical vertebra. T = Cervical trachea. In A–D and F and H, the right side of the image represents the left (L) side of the animal.

Citation: American Journal of Veterinary Research 85, 11; 10.2460/ajvr.24.06.0166

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Four days later, a biopsy of the right adductor mandibulae muscle was acquired at the base of the parietal bone under general anesthesia. The muscle appeared grossly discolored tan and was subjectively firm. Histopathologic evaluation, as interpreted by a board-certified veterinary pathologist (ER), revealed marked loss and fibrosis of skeletal muscle fibers and a mild histiocytic infiltrate (Figure 2). This was accompanied by moderate diffuse histiocytic and granulocytic steatitis. Bacterial and fungal cultures were negative. The animal ate squid rings 29 days after initial trismus presentation, 18 days after methylprednisolone injection, 11 days after starting weekly acupuncture, and 7 days after muscle biopsy. Vitamin E/selenium injections were discontinued, and the turtle continued to show improvements in the range of motion of the jaw and feeding response. Hematologic and plasma biochemical analysis performed 35 days after trismus presentation noted resolution of elevations in CK (89 U/L), LDH (3 U/L), and AST (832 U/L) and resolution of hypoproteinemia (total protein, 3.1 g/dL). Normal range of motion of the jaw was noted 48 days after trismus presentation, and frequency of acupuncture was reduced to every 2 weeks for 2 treatments and then monthly. The turtle subsequently developed diffuse steatitis and osteomyelitis, which prolonged rehabilitation but were successfully managed. Subsequent CT and MRI performed almost 4 months after trismus presentation noted near complete (> 90%) resolution of myositis. The sea turtle was released 8.5 months after admission.

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Histopathology images in cold-stunned Kemp's ridley (Lepidochelys kempii) sea turtles with trismus. Scale bar = 50 µm. A—Histopathology of right adductor mandibulae muscle (case 1). Myofibers are lost and replaced by orange-staining collagen with mild histiocytic infiltrates. Remaining fibers are necrotic or small and atrophic. Hematoxylin phloxine saffron. B—Histopathology of cervical skeletal muscle (case 2). Heterophils (asterisks) infiltrate the muscle and are associated with acute necrosis of individual myofibers (arrowheads). Hematoxylin and eosin. C—Histopathology of mandibular skeletal musculature (case 3). Muscle samples were collected postmortem with frequent regenerating myofibers exhibiting central rowing of nuclei (arrowheads). Hematoxylin and eosin. D—Histopathology of cervical skeletal muscle (case 4). Similarly to case 2 (B), heterophils (asterisks) infiltrate the muscle and are associated with acute necrosis of individual myofibers (arrowhead). Hematoxylin and eosin.

Citation: American Journal of Veterinary Research 85, 11; 10.2460/ajvr.24.06.0166

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Case 2

A 2.4-kg juvenile cold-stunned Kemp's ridley sea turtle with a history of dorsal neck swelling (recorded initially on day 4), signs of weakness (uncoordinated swimming, decreased responsiveness, and inability to lift its head), and severe pneumonia was evaluated on day 12 of rehabilitation for trismus, manifest as staff having difficulty opening the turtle's mouth. Hematologic and plasma biochemical analysis 8 days prior had revealed a mild heterophilic leukocytosis (WBCs, 16.6 k/µL; heterophils, 72%), severely elevated CK (> 120,000 U/L), AST (24,242 U/L), ALP (3,691 U/L), and LDH (> 36,000 U/L). Five jugular venipuncture procedures had been performed before trismus presentation. Medications prescribed included parenteral antimicrobials (Supplementary Table S1), carprofen (1 mg/kg, IM, q 72 h, days 10 to 13), and SC fluid therapy (details not available). The next day the animal was found deceased. On necropsy, craniodorsal cervical muscles were thickened and edematous. Significant histopathologic findings, as interpreted by a board-certified veterinary pathologist (BAS), included severe subacute heterophilic bronchopneumonia with intralesional bacteria and moderate, predominantly heterophilic cervical myositis with associated myonecrosis and hemorrhage (Figure 2).

Case 3

A 25-kg juvenile cold-stunned loggerhead sea turtle with a history of mild pneumonia, bilateral corneal keratopathy, and anorexia since admission presented on day 31 of rehabilitation for minimal appetite and weak attempts to prehend food. Diagnostics including survey radiographs, gastrointestinal contrast radiographs, and blood culture failed to reveal a cause for anorexia. Eleven jugular venipuncture procedures had been performed before presentation. Flunixin meglumine (1 mg/kg, IM, q 72 h, days 24 to 38) had already been prescribed for possible pain and/or inflammation. Levothyroxine (0.04 mg/kg, PO, q 72 h, days 33 to 57) and tube feedings (8 mL/kg herring gruel, procedure as described in case 1, days 31 to 47) were prescribed every 3 days, and parenteral antibiotics (Supplementary Table S1) were continued. Five days later, head tremors and repetitive jaw movements, interpreted as a sign of pain, were noted and tube feedings and flunixin were discontinued. Hematologic and plasma biochemical analysis at this time revealed mild leukocytosis (15.0 K/µL) and mildly elevated CK (16,724 U/L). Computed tomography and MRI were performed by a board-certified veterinary radiologist (JOB), using gadopentetate dimeglumine contrast (75 mg/kg, IV) for MRI. Computed tomography diagnoses included pneumonia in the right caudal lung field and intestinal ileus without obstruction. Magnetic resonance imaging revealed marked multifocal T2 hyperintensity of the left muscles of mastication with smaller foci on the right and marked homogenous enhancement following contrast administration (Figure 1). Six days later, fine needle aspiration of the left adductor mandibulae was unsuccessful. Therapeutic laser therapy (continuous wave, 10 J/cm², 360 J total dose) was initiated, directed posterior to the left eye and craniomedially toward the supraoccipital region, and continued every 3 days. Triamcinolone (0.1 mg/kg, IM) was administered intralesionally once, posterior to the jaw. A Licensed Acupuncturist (CAM) performed 3 acupuncture treatments. The initial 2 treatments were 10 days apart, and the final treatment was a month later. Acupuncture channels with fascial connections to the lateral head and jaw were activated using sterile 38-gauge filiform needles, inserted 3 to 7 mm. Acupuncture points were located on the latissimus dorsi, between the radius and ulna, at the head of the fibula, and on the extremities of the limbs. Each treatment included the following points: LI4, LIV3, TW5, GB34, and GB21.

The animal ate well the day after the first acupuncture treatment and 2 days after triamcinolone injection and continued to eat well for 24 days when the animal's behavior changed, showing a preference for herring filets. Triamcinolone injection was repeated in the same location with no clinical improvement. A CBC revealed mild relative heterophilic leukocytosis (WBCs, 17.0 k/µL; heterophils 74%); plasma biochemical values were normal, and a blood culture was negative. Subsequent MRI (with and without contrast) revealed diffuse muscle changes consistent with myositis of the head and cranial neck. A muscle biopsy was acquired from the dorsal cervical region during recovery from general anesthesia following imaging. Histopathologic evaluation, interpreted by a board-certified veterinary pathologist (BAS), found chronic myopathic change interpreted as severe muscle atrophy, with no evidence of myositis or infectious etiologies. Laser therapy (10 J/cm², 360 J total dose, q 72 h, days 82 to 97), vitamin E/selenium (0.065 mg/kg selenium, 3.25 mg/kg vitamin E, IM, q 6 d, days 91 to 105), flunixin (1 mg/kg, SC, q 72 h, days 94 to 105), and daily SC fluids (lactated Ringer solution) were prescribed. Over the next few days, the animal developed severe coelomic effusion, weight gain, anorexia, lethargy, difficulty surfacing, and multifocal firm SC tissue in the neck, shoulders, prefemoral fossa, and perineum. Radiographs showed evidence of aspiration pneumonia. Due to clinical decline and lack of response to multiple salvage therapies including an additional antimicrobial (Supplementary Table S1) and steroids (stanozolol at 2 mg/kg, IM, once on day 105), the animal was euthanized using pentobarbital at 108 mg/kg, IV. Histopathologic evaluation (BAS) noted diffuse severe, necrotizing steatitis with numerous gram-positive bacterial emboli within adipose tissue; indications of septicemia in multiple organs, including intravascular bacterial emboli in the liver and vasculitis of colonic vessels and mild to moderate bronchopneumonia with intralesional fungi and bacteria. Nonspecific myofiber regeneration consistent with a previous insult was observed within the mandibular musculature. As with the biopsy, there was no evidence of active myositis as suggested by the MRI.

Case 4

A 2.9-kg juvenile cold-stunned Kemp's ridley sea turtle was evaluated 8 days into rehabilitation for intermittently moving the mouth, attempting to swallow, and being unable to open its mouth > 1 cm. Radiographs were consistent with pneumonia. The turtle was treated with parenteral antimicrobials (Supplementary Table S1), SC fluids (lactated Ringer solution; 10 to 20 mL/kg, SC, q 1 to 6 d, with frequency based on serial clinical pathology data, 4 doses, days 8 to 16), vitamin E/selenium (0.065 mg/kg selenium, 3.25 mg/kg vitamin E, IM, q 6 d, days 6 to 17), and ketoprofen (2 mg/kg, IM, q 24 h, days 12 to 17). The turtle received a single physical therapy session and bilateral jaw laser therapy (continuous wave, 10 J/cm², 120 J total dose) daily for 3 doses (days 14 to 17). On day 17, the turtle had moderate soft tissue swelling in the craniodorsal neck, became hypoglycemic and unresponsive, did not respond to medical management, and died naturally. Nine jugular venipuncture procedures had been previously performed. Postmortem muscle biopsies of the craniodorsal cervical muscle were obtained and evaluated by a board-certified veterinary pathologist (BAS). Histopathologic findings included moderate acute heterophilic myositis with myonecrosis, intravascular thrombus formation, and hemorrhage (Figure 2).

Case 5

A 2.76-kg juvenile cold-stunned Kemp's ridley sea turtle was evaluated 12 days into rehabilitation at a long-term care facility and 24 days after rescue in Massachusetts, due to anorexia, tremors when opening its mouth, and inability to open its mouth > 1 cm. Eight venipuncture procedures had been performed before trismus presentation. The turtle had multiple episodes of dull behavior, weakness, and bradycardia over the next 2 weeks. Hematologic and plasma biochemical analysis revealed mild anemia (18% to 21%), a normal total leukocyte count (12.2 k/µL) with immature and toxic heterophils (61%) and vacuolated monocytes (30%), severely elevated CK (> 13,500 U/L) and AST (3,920 U/L), and mild hypoproteinemia (2.4 g/dL). The animal showed interest in eating but was not able to prehend or swallow food. Medications included parenteral and nebulized antibiotics (Supplementary Table S1), fluid therapy (Normosol-R), ketoprofen (2 mg/kg, IM, q 24 h, days 30 to 49), and vitamin E (6.7 mg/kg, IM, q 72 h, days 30 to 100). Mouth opening remained decreased at < 1 cm despite ketoprofen administration for 1 week. Due to persistent anorexia, concerns for progressive hypoproteinemia and fluid overload, and to avoid oral manipulation, fluids were weaned and total parenteral nutrition (TPN; 48 g amino acids [Travasol 10%], 13.5 g dextrose, and 40 g intralipid 20%) at 2.5 mL/kg, IV, was administered every 3 days from days 44 to 59. A CT scan was performed with and without iohexol (1 mL/kg, IV) contrast and interpreted by a board-certified zoological veterinary radiologist (MI). Findings included nonspecific myositis of the dorsal cervical muscles characterized by multifocal bilateral areas of asymmetrical hyperattenuation precontrast, pneumonia, and superficial erosions of the carapace and plastron (Figure 1). Treatment for myositis consisted of a single intralesional injection of methylprednisolone sodium succinate (total dose of 0.8 mg/kg, split among the 2 most severe lesions in the neck via CT and radiographic guidance), serial acupuncture, and physical therapy. Supportive treatments (TPN; antibiotics, antifungals, nebulization) were continued based on the animal's clinical needs. Acupuncture consisted of 15-minute treatments, while the animal underwent nebulization therapy and was performed once daily for the first week, then every 3 days for 6 weeks, and then once weekly until clinical resolution (3 months). Acupuncture channels with fascial connections to the lateral head and jaw were activated using sterile 32-gauge filiform needles inserted less than 10 mm deep at extrapolated meridian points (Yintang, GV20, GV16, LI4, LU07, LI11, BL10, TW5, GB20, and GB21) based on consultation and photographs from the New England Aquarium team (Figure 3). Physical therapy initially consisted of 5 repetitions of 10- to 15-second manual extension of the mouth using carwash strips with equal, opposing pressure (Figure 3) and was performed once daily for the first 5 days, twice daily for 2 weeks, once daily for 6 weeks, and then weaned to 3 times per week and then once weekly until treatment was discontinued.¹⁸ An unaffected Kemp's ridley sea turtle that was concurrently in rehabilitation had a mouth opening of 5 cm, which was used as a point of reference for a normal range of motion.

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Acupuncture therapy (A) for a cold-stunned Kemp's ridley sea turtle (Lepidochelys kempii) sea turtle (case 5) with cervical myositis. Acupuncture at extrapolated meridian points (Yintang, GV20, GV16, LI4, LU07, LI11, BL10, TW5, GB20, and GB21) was performed once daily for the first week, then every 3 days for 6 weeks, and then once weekly until clinical resolution (3 months). Needles were well tolerated and left in place for 15 minutes. Physical therapy (B and C) treatment initially consisted of 5 repetitions of 10 to 15 seconds of manual extension of the mouth using carwash strips with equal, opposing pressure (B). The use of a foam block (C) to stretch the muscles of mastication before manual opening (B) was added once the animal could comfortably open its mouth 3 cm. Physical therapy was performed once daily for the first 5 days, twice daily for 2 weeks, once daily for 6 weeks, and then weaned to 3 times per week and then once weekly until clinical resolution.

Citation: American Journal of Veterinary Research 85, 11; 10.2460/ajvr.24.06.0166

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Only 1 day after methylprednisolone injection, the animal was able to open its mouth 1 cm and ate 6 chopped pieces of squid. The next day, however, the animal was unable to eat again and exhibited floating, quiet behavior. Dexamethasone sodium phosphate (0.1 mg/kg, IM, q 24 h, days 55 to 57) was prescribed for additional anti-inflammatory relief, and hetastarch (5 mL/kg, IV, over 20 minutes, q 4 d, days 50 to 63) was administered to support the animal's persistent hypoproteinemia, in addition to continuing TPN. One week after methylprednisolone injection, the animal was eating 2% body weight in squid and mahi mahi strips and was able to open its mouth 3 cm. Supportive medications (TPN, hetastarch, and dexamethasone) were discontinued; vitamin E was continued along with antimicrobials for concurrent pneumonia. One month into treatment the turtle was voluntarily opening its mouth 3 cm and eating fish. Physical therapy was altered to the use of a foam block to stretch the muscles of mastication before manual opening (Figure 3). Three months after methylprednisolone injection, the mouth opening measured between 4 and 4.5 cm, the turtle was eating all whole fish offered, and CT confirmed the resolution of cervical myositis. The animal continued rehabilitation due to pneumonia and was released 8 months after admission.