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Peripheral neuropathy secondary to a neuroma in an Eastern screech owl (Megascops asio)
Journal of Exotic Pet Medicine 31 (2019) 53 56
Contents lists available at ScienceDirect
Journal of Exotic Pet Medicine journal homepage: www.elsevier.com/locate/jepm
Case Report
Peripheral neuropathy secondary to a neuroma in an Eastern screech owl (Megascops asio) Kristin S. Gill, DVM a,*, Peter J. Helmer, DVM, DABVP (Avian) a, David Gasper, DVM, PhD, DACVP b,c a b c
BluePearl Veterinary Partners, Tampa, FL, USA Zoo/Exotics Pathology Service, Carmichael, CA, USA Pacific Zoo & Wildlife Diagnostics, Vet. Corp. Escondido, CA, USA
A R T I C L E
I N F O
A B S T R A C T
Keywords: Megascops asio Eastern screech owl Neuroma Traumatic neuroma Neuropathic pain Gabapentin
A 1.5-year-old male Eastern screech owl (Megascops asio) was presented for evaluation of a progressive decrease in weight-bearing on a previously injured right leg. Neurologic deficits were noted and progressed despite therapy. A neuroma was diagnosed on necropsy adjacent to the historical femoral malunion. This report describes a presumptive traumatic neuroma of nonartificial origin in a bird with clinical evidence of nerve dysfunction. A symptomatic traumatic neuroma should be considered as a differential in birds with evidence of peripheral neuropathy and a history of injury.
Clinical report
administration was increased (1.5 mg/kg PO q12h) to treat possible orthopedic pain. Three days later, the bird was presented for bleeding from the right foot. The right hallux (digit I) was swollen with a puncture wound at the base of the claw. Superficial pain was assessed; in comparison to the left digits, the owl showed no response to pinching right digits I III, and a weak response to digit IV. The wound was cleaned with sterile saline solution, and trimethoprim-sulfamethoxazole (48 mg/kg PO q12h) was prescribed to control infection. The main differentials for the cause of the injury included incidental trauma, trauma from decreased pain sensation, or self-mutilation from neuropathic pain. Gabapentin was prescribed for the suspected neuropathy; however, the bird was started on a higher dose than recommended (100 mg/kg PO q12h instead of 13 mg/kg PO q12h). For several days, the owl was reported to be minimally active and have a dull mentation. The right leg was still held out at rest. The gabapentin dosage error was noted and decreased to the recommended dose over several days. The bird was presented a week after the initial examination with a new wound on the right foot. Orthopedic evaluation was unchanged. Superficial pain perception was mapped and was absent to digits I III and the medial aspect of the tarsometatarsus, but present to digit IV, the lateral tarsometatarsus, and the leg proximal to the intertarsal joint (Fig. 1). The right foot was swollen and discolored purple with multiple wounds on the hallux. The foot was cleaned and bandaged to protect the soft tissues while healing. All medications were continued. The bird was presented again 11 days after initial examination. The right hallux remained mostly swollen, however, areas around the nail base appeared firm, black, and devitalized. Superficial pain was absent
A 1.5-year-old male Eastern screech owl (Megascops asio) was presented for evaluation of a progressive decrease in weight-bearing on a previously injured right leg. The bird had been determined nonreleasable as a juvenile due to a poorly healed right femoral fracture and glove trained for use in educational presentations. It was housed with another screech owl in an outdoor enclosure. While able to stand upright, the owl had mild gait deficits and preferred to rest with the right leg pronated and the intertarsal joint on the ground. This remained unchanged for a year. The owl was presented for worsening use of its right leg. It had a oneweek history of holding the leg out while on the glove. This initially improved with meloxicam administration (1.5 mg/kg PO q24h), however, 48 hours prior to presentation the bird became reluctant to place weight on the leg again. On physical examination, it was in good body condition (115 g). Orthopedic evaluation of the right leg was unchanged from previous examinations. While physically able to perch and close the toes of the foot with normal strength, the bird shifted weight off the right leg at rest. When the digits were pinched, there was a delayed withdrawal response with digits III and IV and no withdrawal with digits I or II. Proprioception was not assessed. No other abnormalities were noted. The main differentials were pain or a neurologic deficit it was unclear if the owl’s abnormalities were due to pain worsened by weightbearing and motion, or due to neurologic weakness and decreased sensation. Radiographs revealed a previous fracture of the right mid-femoral diaphysis with malunion, and concurrent muscle atrophy. The complete blood cell count and chemistry were unremarkable.1,2 The meloxicam * Corresponding author. Tel.: 813 933 8944; fax: 813 549 7698. E-mail address: [email protected] (K.S. Gill). https://doi.org/10.1053/j.jepm.2019.06.001 1557-5063/© 2019 Elsevier Inc. All rights reserved.
K.S. Gill et al.
Fig. 1. Diagrams of a cranial view (a) and medial view (b) of the owl’s right leg and the areas of superficial sensation loss mapped a week after the initial presentation. The lateral, medial, cranial, and caudal surfaces are marked (L, M, Cr, and Ca, respectively), as well as the digits (I IV). The area shaded in dark gray is the area in which superficial pain sensation was absent.
to all toes. Deep pain was confirmed absent to all toes. Due to suspected repeated self-mutilation and progressive neuropathy, as well as a poor to grave prognosis for leg amputation in an owl,3 the bird was euthanized. At necropsy, the muscles of the right leg were atrophied and the femoral malunion confirmed. A white mass was noted on the lateral aspect of the distal right thigh (Fig. 2a). This arose from a large nerve in the region where the sciatic nerve divided into the fibular and tibial nerves,4 and adjacent to the distal aspect of the previous femoral fracture (Fig 2b). No other abnormalities were noted on gross examination. On histopathology, the mass arose from a large nerve bundle and was composed of haphazardly arranged myelinated nerve fibers separated by proliferative fibroblasts and moderate amounts of collagen (Fig. 3). It contained multiple foci of neuronal degeneration and swelling. Individual acute and subacute myofiber necrosis was noted in the adjacent skeletal muscle, and both the mass and associated blood vessels were infiltrated by aggregates of lymphocytes and plasma cells. The mass was diagnosed as a neuroma, suspected to be a traumatic neuroma secondary to the historical femoral fracture. Discussion Neuromas are benign masses arising from nerves, often secondary to damage (traumatic neuromas). Damaged nerves normally regenerate via the growth of axonal buds. If these are disrupted and cannot reach their targets, the process becomes disorganized and forms a proliferative mass of nerve cells and Schwann cells, a neuroma.5 7 Neuromas are usually relatively firm, white, and slowly growing. When symptomatic they cause nerve deficits and pain.7 9 Traumatic neuromas are reported in human medicine. They are a significant concern and complication of amputation, with reports of the incidence of symptomatic neuromas ranging from 2.7% to 30%.6,10 The major concern in most cases is the development of hypersensitivity and neuropathic pain.11,12 In veterinary medicine, neuromas are one of the common complications of palmar digital neurectomy in horses.7,13,14 They are reported but uncommon in other mammalian species.7 Traumatic neuromas are uncommonly reported in avian medicine. They are a complication and welfare concern of partial beak amputation in chickens5,15 but the prevalence seems to vary with technique, age,
Journal of Exotic Pet Medicine 31 (2019) 53 56
amputation site, and strain.5,16,17 They have not been found in turkeys18 and ducks19,20 after the same procedure. Neuromas have also been reported in chickens secondary to hallux amputation21 but were not present in mynahs after pinioning.22 Outside of these, to the authors’ knowledge1 there is a single report of an ostrich with a suspected traumatic neuroma that formed secondary to a facial laceration.23 This lesion was noted due to a visible mass effect; no evidence of abnormal nerve function was reported.23 Neuromas can lead to hyperalgesia and allodynia increased sensitivity to stimuli. They can also cause neuropathic pain pain that arises from altered function of the nervous system, resulting in ectopic discharges without signal transduction from a stimulus.11 Neuropathic pain is difficult to treat, with a worse prognosis than other forms of pain.11 Human patients describe it as lancing, stabbing, shooting or electriclike, and it can be associated with both sensory and motor nerve deficits.11 It tends to radiate distally, and exacerbations can be common and unpredictable.11 Neuropathic pain is difficult to diagnose, and in human medicine diagnosis relies on communication between the patient and doctor.9 This presents challenges for veterinary medicine, but case reports of suspected neuropathic pain exist. Aside from the previously mentioned concerns of pain secondary to neuromas in chickens, limited reports in avian medicine include a falcon and pigeon. A prairie falcon developed suspected neuropathic pain secondary to a right metacarpal fracture, resulting in self-mutilation of the patagium.24 Treatment was eventually successful and included ketoprofen, gabapentin, ketamine, laser therapy, and a regional block of the radial and medianoulnar nerves.24 Neuropathic pain has also been suspected in a pigeon secondary to granuloma formation at the site of vaccine administration, and treatment was successful with repeated surgical excision, meloxicam, and gabapentin.25 While better studied and reported in psittacine birds, feather destruction and self-mutilation have been reported in raptors.24,26 28 Feather destruction due to boredom in Harris’s hawks appears to be over represented,26,28 but localized self-mutilation after trauma has been reported.24,26,28 Bandage disease was suspected in some of these cases,26 but traumatic neuromas are an alternative differential. Pain control in this owl consisted of two medications: meloxicam and gabapentin. Meloxicam is a COX-2 preferential nonsteroidal anti-inflammatory drug (NSAID) used widely in exotic animal medicine to treat pain via inhibition of prostaglandin production during the inflammatory response.29 Based on the current understanding of the pathophysiology of neuropathic pain, NSAIDs should be ineffective, however, clinical efficacy has been reported in human medicine.11 Pharmacodynamic data for meloxicam has not been reported in owls, but there is a pharmacokinetic study in great horned owls (Bubo virginianus; 0.5 mg/kg PO/IV once).30 A higher dose was used in this bird as pharmacodynamic studies in other avian species have suggested doses in the range of 1 3 mg/kg q12h are necessary for analgesia, with minimal side effects.31,32 Gabapentin is an anticonvulsant drug shown to be effective in treating neuropathic pain in humans.8,33 There are no pharmacodynamic studies in birds. The gabapentin dose in this bird was based on a pharmacokinetic study in great horned owls and the use in the prairie falcon case report.24,33,34 These medications did not stop the self-mutilation or lameness. Neuropathic pain is reported to be frustrating to treat in humans, and
1
PubMed searched using search (neuroma AND (bird* OR aves OR avian*)), Google Scholar first 200 search results for queries (neuroma bird) and (neuroma avian), Google Scholar all results for queries (neuroma strigiformes), (neuroma strigidae), (neuroma owl avian), and (neuroma owl bird), review of neuropathology and oncology sections of major avian texts including Avian Medicine: Principles and Application eds. Ritchie, Harrison and Harrison, Clinical Avian Medicine eds. Harrison and Lightfoot, and Pathology of Pet and Aviary Birds 2nd edition by Schmidt, Reavill and Phalen.
K.S. Gill et al.
Journal of Exotic Pet Medicine 31 (2019) 53 56
Fig. 2. The legs of the owl during gross post-mortem examination. (a) Lateral view of the abnormal right leg (R) after dissection, with a lateral view of the normal left leg (L) for comparison. The arrow indicates the mass. The sciatic nerve (S, aka ischiatic nerve), fibular nerve (F, aka peroneal nerve), and tibial nerve (T) are marked in the left leg for clarity. The digits are also identified (I IV) on each foot, with the damage to the right hallux (digit I) visible. (b) Lateral view of the area of the mass. The area of the previous femoral fracture malunion (FF) is identified adjacent to the mass of nerve tissue (M) lateral to the distal femur and stifle joint. The nerves are again indicated.
Fig. 3. Microscopic images of the neuroma. (a) Subgross image depicting a mass of haphazardly arranged myelinated nerve fibers surrounded by connective tissue (collagen fibers and adipose). Associated skeletal muscle is present in the lower right; myofiber necrosis is not present in this section. Focal regions of inflammation (*) characterized by lymphocytes and plasma cells are scattered throughout the tissues depicted. (b) Higher magnification (40×) image of the neuroma, showing a mixed population of nerve bundles and support cells (predominantly Schwann cells, along with endoneurial and perineurial fibroblasts and pericytes). Hematoxylin and eosin stains.
therapeutic options include pharmacotherapy, nerve blocks, nerve ablation, physical therapy and massage, electrotherapy or transcutaneous magnetic stimulation, and surgical resection.8,9,35,36 With symptomatic neuromas, generally surgical treatment is recommended after medical management has failed.8,37 An NSAID and gabapentin were part of successful therapy in the prairie falcon and pigeon; additional therapies included ketamine, a nerve block, laser therapy, and surgical resection of the diseased tissue.24,25 It is unknown if the addition of these treatments would have benefited the owl. Instead it was euthanized as continued trial therapy with a declining quality of life and unknown prognosis was deemed unfair by the owner and authors. Of note is that the owl did not mutilate at higher gabapentin doses. This was also noted in the prairie falcon case report the starting dose (11 mg/kg PO q12h) was ineffective, but a higher dose was a component of successful therapy (82 mg/kg PO q12).24 A dose of approximately 100 mg/kg was also reported in both birds, and while both exhibited dull mentation, only the falcon displayed diarrhea and ataxia.24 The owl was suspected to have paused its mutilation on this dose due to sedation and not pain control as it had remained lame. The owl lost superficial pain sensation in distinct regions of the right leg. Autonomous zones are areas of skin innervated by a single nerve,
and used to test for nerve dysfunction via loss of sensation to that area.7 The specific areas vary between species.38 Autonomous zones have not been reported in any avian species.2 This is the first report of a neuroma in an owl or in the thigh of a bird. Given the proximity to a previous injury, this is the second report in birds of a suspected traumatic neuroma of non-artificial origin,23 and the first with evidence of being a symptomatic neuroma. More importantly, this case serves as a reminder of the challenges in treating neuropathic pain. In a human, after medical management failed to control discomfort, the next step likely would have been surgical resection of the neuroma. It is unknown if surgical care would have helped this bird, but due to the lack of reports of neuromas in birds and the presence of the mass far proximal to the affected sites, a neuroma was not suspected, and surgical exploration likely would have been in the denervated areas and missed the lesion. This case also demonstrates what was likely an
2
PubMed searched using search ((“autonomous zone*” OR “cutaneous area*” OR “cutaneous innervation”) AND (bird* OR aves OR avian* OR veterin*)), Google Scholar all results for queries (“autonomous zone” avian) and (“cutaneous area” avian).
K.S. Gill et al.
autogenous zone for the sciatic, fibular, or tibial nerve in the screech owl; further mapping of autogenous zones in birds are needed to better diagnose and treat peripheral neuropathies. Further studies are needed of treatment options for neuropathic pain in all species. References 1. Hawkins MG, Guzman DS, Beaufrere H, Lennox AM, Carpenter JW: Birds, in Carpenter JW, Marion C (eds): Exot. Anim. Formul. (ed 5). St. Louis, MO, Elsevier Inc., pp 167–375, 2018 2. Ammersbach M, Beaufr ere H, Gionet Rollick A, Tully T: Laboratory blood analysis in Strigiformes-Part I: hematologic reference intervals and agreement between manual blood cell counting techniques. Vet Clin Pathol 44:94–108, 2015. https://doi.org/ 10.1111/vcp.12229 3. Park F: Behavior and behavioral problems of Australian raptors in captivity. Semin Avian Exot Pet Med 12:232–241, 2003. https://doi.org/10.1053/S1055-937X(03)00038-0 4. Orosz SE, Ensley PK, Haynes CJ: Avian Surgical Anatomy: Thoracic and Pelvic Limbs. Philadelphia, W. B. Saunders Company, 1992 5. Kuenzel WJ: Neurobiological basis of sensory perception: welfare implications of beak trimming. Poult Sci 86:1273–1282, 2007. https://doi.org/10.1093/ps/86.6.1273 6. Vlot MA, Wilkens SC, Chen NC, Eberlin KR: Symptomatic neuroma following initial amputation for traumatic digital amputation. J Hand Surg Am 43:86.e1–86.e8, 2018. https://doi.org/10.1016/j.jhsa.2017.08.021 7. DeLahunta A, Glass E: Veterinary Neuroanatomy and Clinical Neurology. (ed 3). St. Louis, MO, Saunders, 2009 8. Yao C, Zhou X, Zhao B, Sun C, Poonit K, Yan H: Treatments of traumatic neuropathic pain: a systematic review. Oncotarget 8:57670–57679, 2017. https://doi.org/ 10.18632/oncotarget.16917 9. Hanna SA, Catapano J, Borschel GH: Painful pediatric traumatic neuroma: surgical management and clinical outcomes. Childs Nerv Syst 32:1191–1194, 2016. https:// doi.org/10.1007/s00381-016-3109-z 10. Van Der Avoort DJJC, Hovius SER, Selles RW, Van Neck JW, Coert JH: The incidence of symptomatic neuroma in amputation and neurorrhaphy patients. Br J Plast Surg 66:1330–1334, 2013. https://doi.org/10.1016/j.bjps.2013.06.019 11. Cohen SP, Mao J: Neuropathic pain: mechanisms and their clinical implications. BMJ 348:f7656, 2014. https://doi.org/10.1136/bmj.f7656 12. Schug SA, Gillespie G: Post-amputation pain, in Fitridge R, Thompson M (eds): Mech Vasc Dis A Ref B Vasc Spec. Adelaide, Barr Smith Press, pp 389–400, 2011 13. Matthews S, Dart AJ, Dowling BA: Palmar digital neurectomy in 24 horses using the guillotine technique. Aust Vet J 81:402–405, 2003. https://doi.org/10.1111/j.17510813.2003.tb11545.x 14. Maher O, Davis DM, Drake C, et al: Pull-through technique for palmar digital neurectomy: forty-one horses (1998-2004). Vet Surg 37:87–93, 2008. https://doi.org/ 10.1111/j.1532-950X.2007.00352.x 15. Gentle MJ: Neuroma formation following partial beak amputation (beak trimming) in the chicken. Res Vet Sci 41:383–385, 1986. https://doi.org/10.1016/S0034-5288(18)30635-0 16. Schwean-Lardner K, Annett-Christianson CB, Rajendram J, Classen HL: Does age of hot-blade trimming impact the performance and welfare of 2 strains of White Leghorn hens? J Appl Poult Res 25:547–560, 2016. https://doi.org/10.3382/japr/pfw037 17. Lunam C, Glatz P, Hsu Y-J: The absence of neuromas in beaks of adult hens after conservative trimming at hatch. Aust Vet J 7:46–49, 1996. https://doi.org/10.1111/ j.1751-0813.1996.tb13734.x 18. Gentle MJ, Thorp BH, Hughes BO: Anatomical consequences of partial beak amputation (beak trimming) in turkeys. Res Vet Sci 58:158–162, 1995. https://doi.org/ 10.1016/0034-5288(95)90070-5
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19. Gustafson LA, Cheng HW, Garner JP, Pajor EA, Mench JA: The effects of different billtrimming methods on the well-being of Pekin ducks. Poult Sci 86:1831–1839, 2007. https://doi.org/10.1093/ps/86.9.1831 20. Gustafson LA, Cheng HW, Garner JP, Pajor EA, Mench JA: Effects of bill-trimming Muscovy ducks on behavior, body weight gain, and bill morphopathology. Appl Anim Behav Sci 103:59–74, 2007. https://doi.org/10.1016/j. applanim.2006.04.003 21. Gentle MJ, Hunter LH: Neural consequences of partial toe amputation in chickens. Res Vet Sci 45:374–376, 1988. https://doi.org/10.1016/S0034-5288(18)30968-8 22. Peng SJ, Judy FC, Fei SIAC: Welfare assessment of flight-restrained captive birds: effects of inhibition of locomotion. Thai J Vet Med 43:235–241, 2013 23. Tully TN, Mcclure JR, Morris JM, Cho D-Y: Post-transectional submandibular neuroma in an Ostrich (Struthio camelus). J Assoc Avian Vet 7:75–76, 1993. https://doi.org/ 10.2307/30135006 24. Shaver SL, Robinson NG, Wright BD, Kratz GE, Johnston MS: A multimodal approach to management of suspected neuropathic pain in a Prairie Falcon (Falco mexicanus). J Avian Med Surg 23:209–213, 2009. https://doi.org/10.1647/2008-038.1 25. Cowan ML, Monks DJ, Raidal SR: Granuloma formation and suspected neuropathic pain in a domestic pigeon (Columba livia) secondary to an oil-based, inactivated Newcastle disease vaccine administered for protection against pigeon paramyxovirus-1. Aust Vet J 92:171–176, 2014. https://doi.org/10.1111/avj.12173 26. Smith SP, Forbes NA: A novel technique for prevention of self-mutilation in three Harris’ hawks (Parabuteo unicinctus). J Avian Med Surg 23:49–53, 2009. https://doi. org/10.1647/2005-046R1.1 27. Chitty J: Feather plucking/chewing in raptors. Proc Annu Conf Assoc Avian Vet 91–94, 2005 28. Jones MP: Behavioral aspects of captive birds of prey. Vet Clin North Am Exot Anim Pract 4:613–632, 2001. https://doi.org/10.1016/S1094-9194(17)30026-9 29. Kirchgessner MS: Therapeutic review: meloxicam. J Exot Pet Med 16:281–283, 2007. https://doi.org/10.1053/j.jepm.2006.09.009 30. Lacasse C, Gamble KC, Boothe DM: Pharmacokinetics of a single dose of intravenous and oral meloxicam in red-tailed hawks (Buteo jamaicencis) and great horned owls (Bubo virginianus). J Avian Med Surg 27:204–210, 2013. https://doi.org/10.1647/ 2012-044 31. Cole GA, Paul-Murphy J, Krugner-Higby L, et al: Analgesic effects of intramuscular administration of meloxicam in Hispaniolan parrots (Amazona ventralis) with experimentally induced arthritis. Am J Vet Res 235:1436, 2009. https://doi.org/10.2460/ javma.235.12.1436 32. Desmarchelier M, Troncy E, Fitzgerald G, Lair S: Analgesic effects of meloxicam administration on postoperative orthopedic pain in domestic pigeons (Columba livia). Am J Vet Res 73:361–367, 2012. https://doi.org/10.2460/ajvr.73.3.361 33. Berg K: Therapeutic review: gabapentin. J Exot Pet Med 27:78–81, 2018. https://doi. org/10.1053/j.jepm.2018.07.002 34. Yaw T, Zaffarano B, Gall A, et al: Pharmacokinetic properties on a single administration of oral gabapentin in the great horned owl (Bubo virginianus). J Zoo Wildl Med 46:547–552, 2015. https://doi.org/10.1638/2015-0018.1 35. Kang J, Yang P, Zang Q, He X: Traumatic neuroma of the superficial peroneal nerve in a patient: a case report and review of the literature. World J Surg Oncol 14:242, 2016. https://doi.org/10.1186/s12957-016-0990-6 36. Domeshek LF, Kraus EM, Snyder-Warwick AK, et al: Surgical treatment of neuromas improved patient-reported pain, depression and quality of life. Plast Reconstr Surg J 139:407–418, 2017. https://doi.org/10.1097/PRS.0000000000003018 37. Poppler LH, Parikh RP, Bichanich MJ, et al: Surgical interventions for the treatment of painful neuroma. Pain 159:214–223, 2018. https://doi.org/10.1097/j. pain.0000000000001101 38. Levine JM, Levine GJ, Hoffman AG, Mez J, Bratton GR: Comparative anatomy of the horse, ox, and dog : the vertebral column. Compend Equine: 279–292, 2007
Contents lists available at ScienceDirect
Journal of Exotic Pet Medicine journal homepage: www.elsevier.com/locate/jepm
Case Report
Peripheral neuropathy secondary to a neuroma in an Eastern screech owl (Megascops asio) Kristin S. Gill, DVM a,*, Peter J. Helmer, DVM, DABVP (Avian) a, David Gasper, DVM, PhD, DACVP b,c a b c
BluePearl Veterinary Partners, Tampa, FL, USA Zoo/Exotics Pathology Service, Carmichael, CA, USA Pacific Zoo & Wildlife Diagnostics, Vet. Corp. Escondido, CA, USA
A R T I C L E
I N F O
A B S T R A C T
Keywords: Megascops asio Eastern screech owl Neuroma Traumatic neuroma Neuropathic pain Gabapentin
A 1.5-year-old male Eastern screech owl (Megascops asio) was presented for evaluation of a progressive decrease in weight-bearing on a previously injured right leg. Neurologic deficits were noted and progressed despite therapy. A neuroma was diagnosed on necropsy adjacent to the historical femoral malunion. This report describes a presumptive traumatic neuroma of nonartificial origin in a bird with clinical evidence of nerve dysfunction. A symptomatic traumatic neuroma should be considered as a differential in birds with evidence of peripheral neuropathy and a history of injury.
Clinical report
administration was increased (1.5 mg/kg PO q12h) to treat possible orthopedic pain. Three days later, the bird was presented for bleeding from the right foot. The right hallux (digit I) was swollen with a puncture wound at the base of the claw. Superficial pain was assessed; in comparison to the left digits, the owl showed no response to pinching right digits I III, and a weak response to digit IV. The wound was cleaned with sterile saline solution, and trimethoprim-sulfamethoxazole (48 mg/kg PO q12h) was prescribed to control infection. The main differentials for the cause of the injury included incidental trauma, trauma from decreased pain sensation, or self-mutilation from neuropathic pain. Gabapentin was prescribed for the suspected neuropathy; however, the bird was started on a higher dose than recommended (100 mg/kg PO q12h instead of 13 mg/kg PO q12h). For several days, the owl was reported to be minimally active and have a dull mentation. The right leg was still held out at rest. The gabapentin dosage error was noted and decreased to the recommended dose over several days. The bird was presented a week after the initial examination with a new wound on the right foot. Orthopedic evaluation was unchanged. Superficial pain perception was mapped and was absent to digits I III and the medial aspect of the tarsometatarsus, but present to digit IV, the lateral tarsometatarsus, and the leg proximal to the intertarsal joint (Fig. 1). The right foot was swollen and discolored purple with multiple wounds on the hallux. The foot was cleaned and bandaged to protect the soft tissues while healing. All medications were continued. The bird was presented again 11 days after initial examination. The right hallux remained mostly swollen, however, areas around the nail base appeared firm, black, and devitalized. Superficial pain was absent
A 1.5-year-old male Eastern screech owl (Megascops asio) was presented for evaluation of a progressive decrease in weight-bearing on a previously injured right leg. The bird had been determined nonreleasable as a juvenile due to a poorly healed right femoral fracture and glove trained for use in educational presentations. It was housed with another screech owl in an outdoor enclosure. While able to stand upright, the owl had mild gait deficits and preferred to rest with the right leg pronated and the intertarsal joint on the ground. This remained unchanged for a year. The owl was presented for worsening use of its right leg. It had a oneweek history of holding the leg out while on the glove. This initially improved with meloxicam administration (1.5 mg/kg PO q24h), however, 48 hours prior to presentation the bird became reluctant to place weight on the leg again. On physical examination, it was in good body condition (115 g). Orthopedic evaluation of the right leg was unchanged from previous examinations. While physically able to perch and close the toes of the foot with normal strength, the bird shifted weight off the right leg at rest. When the digits were pinched, there was a delayed withdrawal response with digits III and IV and no withdrawal with digits I or II. Proprioception was not assessed. No other abnormalities were noted. The main differentials were pain or a neurologic deficit it was unclear if the owl’s abnormalities were due to pain worsened by weightbearing and motion, or due to neurologic weakness and decreased sensation. Radiographs revealed a previous fracture of the right mid-femoral diaphysis with malunion, and concurrent muscle atrophy. The complete blood cell count and chemistry were unremarkable.1,2 The meloxicam * Corresponding author. Tel.: 813 933 8944; fax: 813 549 7698. E-mail address: [email protected] (K.S. Gill). https://doi.org/10.1053/j.jepm.2019.06.001 1557-5063/© 2019 Elsevier Inc. All rights reserved.
K.S. Gill et al.
Fig. 1. Diagrams of a cranial view (a) and medial view (b) of the owl’s right leg and the areas of superficial sensation loss mapped a week after the initial presentation. The lateral, medial, cranial, and caudal surfaces are marked (L, M, Cr, and Ca, respectively), as well as the digits (I IV). The area shaded in dark gray is the area in which superficial pain sensation was absent.
to all toes. Deep pain was confirmed absent to all toes. Due to suspected repeated self-mutilation and progressive neuropathy, as well as a poor to grave prognosis for leg amputation in an owl,3 the bird was euthanized. At necropsy, the muscles of the right leg were atrophied and the femoral malunion confirmed. A white mass was noted on the lateral aspect of the distal right thigh (Fig. 2a). This arose from a large nerve in the region where the sciatic nerve divided into the fibular and tibial nerves,4 and adjacent to the distal aspect of the previous femoral fracture (Fig 2b). No other abnormalities were noted on gross examination. On histopathology, the mass arose from a large nerve bundle and was composed of haphazardly arranged myelinated nerve fibers separated by proliferative fibroblasts and moderate amounts of collagen (Fig. 3). It contained multiple foci of neuronal degeneration and swelling. Individual acute and subacute myofiber necrosis was noted in the adjacent skeletal muscle, and both the mass and associated blood vessels were infiltrated by aggregates of lymphocytes and plasma cells. The mass was diagnosed as a neuroma, suspected to be a traumatic neuroma secondary to the historical femoral fracture. Discussion Neuromas are benign masses arising from nerves, often secondary to damage (traumatic neuromas). Damaged nerves normally regenerate via the growth of axonal buds. If these are disrupted and cannot reach their targets, the process becomes disorganized and forms a proliferative mass of nerve cells and Schwann cells, a neuroma.5 7 Neuromas are usually relatively firm, white, and slowly growing. When symptomatic they cause nerve deficits and pain.7 9 Traumatic neuromas are reported in human medicine. They are a significant concern and complication of amputation, with reports of the incidence of symptomatic neuromas ranging from 2.7% to 30%.6,10 The major concern in most cases is the development of hypersensitivity and neuropathic pain.11,12 In veterinary medicine, neuromas are one of the common complications of palmar digital neurectomy in horses.7,13,14 They are reported but uncommon in other mammalian species.7 Traumatic neuromas are uncommonly reported in avian medicine. They are a complication and welfare concern of partial beak amputation in chickens5,15 but the prevalence seems to vary with technique, age,
Journal of Exotic Pet Medicine 31 (2019) 53 56
amputation site, and strain.5,16,17 They have not been found in turkeys18 and ducks19,20 after the same procedure. Neuromas have also been reported in chickens secondary to hallux amputation21 but were not present in mynahs after pinioning.22 Outside of these, to the authors’ knowledge1 there is a single report of an ostrich with a suspected traumatic neuroma that formed secondary to a facial laceration.23 This lesion was noted due to a visible mass effect; no evidence of abnormal nerve function was reported.23 Neuromas can lead to hyperalgesia and allodynia increased sensitivity to stimuli. They can also cause neuropathic pain pain that arises from altered function of the nervous system, resulting in ectopic discharges without signal transduction from a stimulus.11 Neuropathic pain is difficult to treat, with a worse prognosis than other forms of pain.11 Human patients describe it as lancing, stabbing, shooting or electriclike, and it can be associated with both sensory and motor nerve deficits.11 It tends to radiate distally, and exacerbations can be common and unpredictable.11 Neuropathic pain is difficult to diagnose, and in human medicine diagnosis relies on communication between the patient and doctor.9 This presents challenges for veterinary medicine, but case reports of suspected neuropathic pain exist. Aside from the previously mentioned concerns of pain secondary to neuromas in chickens, limited reports in avian medicine include a falcon and pigeon. A prairie falcon developed suspected neuropathic pain secondary to a right metacarpal fracture, resulting in self-mutilation of the patagium.24 Treatment was eventually successful and included ketoprofen, gabapentin, ketamine, laser therapy, and a regional block of the radial and medianoulnar nerves.24 Neuropathic pain has also been suspected in a pigeon secondary to granuloma formation at the site of vaccine administration, and treatment was successful with repeated surgical excision, meloxicam, and gabapentin.25 While better studied and reported in psittacine birds, feather destruction and self-mutilation have been reported in raptors.24,26 28 Feather destruction due to boredom in Harris’s hawks appears to be over represented,26,28 but localized self-mutilation after trauma has been reported.24,26,28 Bandage disease was suspected in some of these cases,26 but traumatic neuromas are an alternative differential. Pain control in this owl consisted of two medications: meloxicam and gabapentin. Meloxicam is a COX-2 preferential nonsteroidal anti-inflammatory drug (NSAID) used widely in exotic animal medicine to treat pain via inhibition of prostaglandin production during the inflammatory response.29 Based on the current understanding of the pathophysiology of neuropathic pain, NSAIDs should be ineffective, however, clinical efficacy has been reported in human medicine.11 Pharmacodynamic data for meloxicam has not been reported in owls, but there is a pharmacokinetic study in great horned owls (Bubo virginianus; 0.5 mg/kg PO/IV once).30 A higher dose was used in this bird as pharmacodynamic studies in other avian species have suggested doses in the range of 1 3 mg/kg q12h are necessary for analgesia, with minimal side effects.31,32 Gabapentin is an anticonvulsant drug shown to be effective in treating neuropathic pain in humans.8,33 There are no pharmacodynamic studies in birds. The gabapentin dose in this bird was based on a pharmacokinetic study in great horned owls and the use in the prairie falcon case report.24,33,34 These medications did not stop the self-mutilation or lameness. Neuropathic pain is reported to be frustrating to treat in humans, and
1
PubMed searched using search (neuroma AND (bird* OR aves OR avian*)), Google Scholar first 200 search results for queries (neuroma bird) and (neuroma avian), Google Scholar all results for queries (neuroma strigiformes), (neuroma strigidae), (neuroma owl avian), and (neuroma owl bird), review of neuropathology and oncology sections of major avian texts including Avian Medicine: Principles and Application eds. Ritchie, Harrison and Harrison, Clinical Avian Medicine eds. Harrison and Lightfoot, and Pathology of Pet and Aviary Birds 2nd edition by Schmidt, Reavill and Phalen.
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Fig. 2. The legs of the owl during gross post-mortem examination. (a) Lateral view of the abnormal right leg (R) after dissection, with a lateral view of the normal left leg (L) for comparison. The arrow indicates the mass. The sciatic nerve (S, aka ischiatic nerve), fibular nerve (F, aka peroneal nerve), and tibial nerve (T) are marked in the left leg for clarity. The digits are also identified (I IV) on each foot, with the damage to the right hallux (digit I) visible. (b) Lateral view of the area of the mass. The area of the previous femoral fracture malunion (FF) is identified adjacent to the mass of nerve tissue (M) lateral to the distal femur and stifle joint. The nerves are again indicated.
Fig. 3. Microscopic images of the neuroma. (a) Subgross image depicting a mass of haphazardly arranged myelinated nerve fibers surrounded by connective tissue (collagen fibers and adipose). Associated skeletal muscle is present in the lower right; myofiber necrosis is not present in this section. Focal regions of inflammation (*) characterized by lymphocytes and plasma cells are scattered throughout the tissues depicted. (b) Higher magnification (40×) image of the neuroma, showing a mixed population of nerve bundles and support cells (predominantly Schwann cells, along with endoneurial and perineurial fibroblasts and pericytes). Hematoxylin and eosin stains.
therapeutic options include pharmacotherapy, nerve blocks, nerve ablation, physical therapy and massage, electrotherapy or transcutaneous magnetic stimulation, and surgical resection.8,9,35,36 With symptomatic neuromas, generally surgical treatment is recommended after medical management has failed.8,37 An NSAID and gabapentin were part of successful therapy in the prairie falcon and pigeon; additional therapies included ketamine, a nerve block, laser therapy, and surgical resection of the diseased tissue.24,25 It is unknown if the addition of these treatments would have benefited the owl. Instead it was euthanized as continued trial therapy with a declining quality of life and unknown prognosis was deemed unfair by the owner and authors. Of note is that the owl did not mutilate at higher gabapentin doses. This was also noted in the prairie falcon case report the starting dose (11 mg/kg PO q12h) was ineffective, but a higher dose was a component of successful therapy (82 mg/kg PO q12).24 A dose of approximately 100 mg/kg was also reported in both birds, and while both exhibited dull mentation, only the falcon displayed diarrhea and ataxia.24 The owl was suspected to have paused its mutilation on this dose due to sedation and not pain control as it had remained lame. The owl lost superficial pain sensation in distinct regions of the right leg. Autonomous zones are areas of skin innervated by a single nerve,
and used to test for nerve dysfunction via loss of sensation to that area.7 The specific areas vary between species.38 Autonomous zones have not been reported in any avian species.2 This is the first report of a neuroma in an owl or in the thigh of a bird. Given the proximity to a previous injury, this is the second report in birds of a suspected traumatic neuroma of non-artificial origin,23 and the first with evidence of being a symptomatic neuroma. More importantly, this case serves as a reminder of the challenges in treating neuropathic pain. In a human, after medical management failed to control discomfort, the next step likely would have been surgical resection of the neuroma. It is unknown if surgical care would have helped this bird, but due to the lack of reports of neuromas in birds and the presence of the mass far proximal to the affected sites, a neuroma was not suspected, and surgical exploration likely would have been in the denervated areas and missed the lesion. This case also demonstrates what was likely an
2
PubMed searched using search ((“autonomous zone*” OR “cutaneous area*” OR “cutaneous innervation”) AND (bird* OR aves OR avian* OR veterin*)), Google Scholar all results for queries (“autonomous zone” avian) and (“cutaneous area” avian).
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