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A Retrospective Study of Horner Syndrome in Australian Wild Birds, 2010-2016.

Abstract: Horner syndrome was identified in 25 of 30 777 avian admissions to Currumbin Wildlife Hospital during 2010-2016. Unilateral ptosis and erection of facial feathers were distinct findings on physical examination and consistent across 9 species. Affected birds were biased toward adults (64%) suffering traumatic injuries (88%). Concurrent injuries requiring treatment were present in 38% of cases, and 76% had additional neurologic deficits. Prognosis for release was poor, with an overall success rate of 32%. Resolution of clinical signs increased to 44% with higher doses of meloxicam and required an average hospitalization of 22 days (range, 3-78 days). Further investigation of the underlying causes of Horner syndrome in birds to provide treatment and prognostic guidelines is warranted.

Key words: Horner syndrome, trauma, sympathetic nervous system, ptosis, bird, avian

Introduction

Horner syndrome, or oculosympathetic paresis, results from any interruption of the 3-neuron pathway of the oculosympathetic tract from the brain to the eye and adjacent structures. (1,2) Clinical signs described in birds are ptosis and contralateral erection of facial feathers with or without miosis. (3)

Unilateral Horner syndrome has been reported in an African spotted eagle owl (Bubo africanus) with ptosis and mild miosis; an eastern screech owl (Megascops asio) with ptosis, facial feather asymmetry, and mild miosis; and a red-bellied parrot (Poicephalus rufiventris) with ptosis and facial feather asymmetry without miosis. (3-5) Central and peripherally induced Horner syndrome have also been induced experimentally in domestic fowl and the house finch (Carpodacus mexicanus), respectively. (6,7)

The oculosympathetic tract has been well described in birds. (3) Sympathetic supply originates at the hypothalamus and traverses the thoracolumbar spinal cord and cranial cervical ganglion to innervate the eye, vasculature, and feather follicles of the head and neck. (3,6) Facial asymmetry caused by unilateral ptosis and erection of facial feathers is induced by loss of adrenergic innervation of the smooth muscle of the eyelids and feathers. (6,8,9)

Based on the few published reports of Horner syndrome in birds, the condition is assumed rare or difficult to identify. (3) The purpose of this study was to report the occurrence, clinical history, and outcome of wild birds presenting with Horner syndrome.

Materials and Methods

The medical records from all avian admissions to the Currumbin Wildlife Hospital between August 10, 2010, and December 8, 2016, were retrospectively reviewed. The 30 777 cases were extracted into Microsoft Excel (Microsoft, Redmond, WA, USA) for analysis, and 25 cases were identified with a diagnosis of Horner syndrome and consistent clinical notes. Extracted case data included accession number, time of accession, history, admission notes, weight on arrival, age, species, duration of hospitalization, diagnosis, and treatment notes.

All affected birds were subject to distance observation and physical examination, followed by examination under general anaesthesia and complete body radiographs once each patient was deemed stable. Horner syndrome was defined in this study as ptosis and ipsilateral erection of facial feathers, with or without miosis.

Results

A total of 25 birds were diagnosed with Horner syndrome during the 6-year period, yielding an admission rate of 1 case per 1231 admissions (Table 1). Clinical signs of ptosis and asymmetric erection of facial feathers were quite distinct on physical examination and were consistent across species (Figs 1 and 2). Time and month of admission were highly variable among cases with no clear seasonality or temporal pattern.

Species affected included rainbow lorikeet (Trichoglossus haematodus), scaly breasted lorikeet (Trichoglossus chlorolepidotus), tawny frogmouth (Podargus strigoides), southern boobook (Ninox novaeseelandiae), laughing kookaburra (Dacelo novaeguineae), crested tern (Thalasseus bergii), crested pigeon (Ocyphaps lophotes), Torresian crow (Corvus orru), and grey butcherbird (Cracticus torquatus) (Table 2). Birds were more likely to be adults (64%; n = 16) than subadults (36%; n = 9), and Horner syndrome was not observed in any juvenile birds. Affected rainbow lorikeets, the most commonly affected species, represented 0.2% (13 of 7069) of all rainbow lorikeets admitted to Currumbin Wildlife Hospital with a primary diagnosis of trauma during the study period.

The most common reasons for presentation were "found on ground" (40%; n = 10), "unable to fly" (20%; n = 5), "window strike" (12%; n = 3), and "vehicle impact" (8%; n = 2). The remainder included "cat attack," "found in swimming pool," and "unknown." Most cases were admitted for traumatic injuries (88%; n = 22); however, a single case (4%) was affected by psittacine beak and feather disease, and in 2 cases (8%), the primary cause was undetermined.

All cases of Horner syndrome were unilateral, reported as left (40%; n = 10), right (32%; n = 8), or not recorded (28%; n = 7). Concurrent traumatic injuries were reported in 10 cases (40%) and were ipsilateral to the Horner syndrome when restricted to one side. There were 14 cases (56%) that demonstrated altered demeanor, and 19 (76%) had concurrent neurologic deficits (Table 3).

Of the 25 birds with Horner syndrome, 8 (32%) were released and 17 (68%) were euthanatized or died. The species most likely to be released were scaly breasted lorikeets (50%; 2 of 4), rainbow lorikeets (38%; 5 of 13), and tawny frogmouths (50%; 1 of 2), whereas all other species died or were euthanatized during treatment. Outcome was not affected by age, with a likelihood of release of 31% (5 of 16) and 33% (3 of 9) for adults and subadults, respectively. Survivors spent between 3 and 78 days in the hospital, with a median of 7 days and an average of 22 days.

All cases were treated with parenteral meloxicam during the initial assessment, followed by oral meloxicam twice daily until symptoms resolved. Meloxicam dose rates were split chronologically within the group, with cases 1-7 receiving 0.2 mg/ kg and cases 8-25 receiving 1 mg/kg because of a revision in hospital treatment protocols. Cases 1-7 had a 0% survival rate and a mean hospitalization time of 55 hours (range, 24-102 hours). Cases 8-25 had a survival rate of 44%, with a mean hospitalization time of 517 hours (range, 68-1867 hours) and 17.5 hours (range, 0-96 hours) for released and fatal cases, respectively.

Discussion

This is the first retrospective study, to our knowledge, of Horner syndrome in birds and confirms ptosis and the asymmetric erection of feathers as consistent clinical signs. The few observed cases suggests that Horner syndrome is a rare condition, even among species such as rainbow lorikeets, which are frequently observed with traumatic injuries. This is consistent with the scarcity of published reports of Horner syndrome among birds. In comparison, a 40-year study of Horner syndrome in people younger than 19 years reported an incidence of 1.42 per 100 000 cases, which is significantly less common than the 81.23 per 100 000 cases reported in wild birds here. (1) Aalbers et al (10) reported that 68% of rats developed Horner syndrome after experimental carotid surgery; however, the incidence of Horner syndrome in other species and naturally occurring cases is unknown.

All cases in this study demonstrated very obvious facial asymmetry caused by ptosis and feather erection on physical examination. More subtle cases may have been overlooked, leading to an underestimate of Horner cases; however, our findings suggest that the condition has been underreported in the literature. Classic signs of Horner syndrome in mammals are miosis and ptosis, with or without concurrent anhidrosis, iris heterochromia, and pupillary dilation lag. (1) Ptosis and erection of facial feathers appear to be consistent clinical signs among captive and wild birds, whereas miosis is variable and anhidrosis is not a feature of birds. (3)

Horner syndrome has been reported in dogs, cats, birds, rats, horses, cows, pigs, sheep, goats, and people. (2,3,10-12) Common causes in mammalian species relate to trauma, inflammation, or impingement of the 3-neuron oculosympathetic pathway. Horner syndrome in cats was commonly associated with a diagnosis of focal trauma, infection or inflammation, neoplasia, or idiopathic. (13) Reported causes in dogs are otitis media and interna; neoplasia of the thorax, thyroid, brain, and vagal nerve; intrathoracic tube displacement; encephalitis; intervertebral disc disease; and trauma to the head, neck, thorax and brachial plexus, and trigeminal nerve. (14) Half of all reported canine and human cases are idiopathic, and 10% of nonidiopathic human cases are iatrogenic. (14-16) In adult humans, traumatic carotid or vertebral artery dissection, cervical adenopathy, neck and spinal surgery, congenital abnormalities, and infection are common causes. (1,17) In children, Horner syndrome is most commonly congenital, including birth trauma, vascular malformations, and neoplasia. (1) Although an anatomic diagnosis was not pursued for cases in the present study, further investigation by imaging or necropsy may provide additional information on the occurrence of arterial damage or the presence of tumors.

Acquired Horner syndrome was the most likely cause of neuropathy in each of the wild bird cases presented. Trauma is common among birds presented to the wildlife hospital, caused by window strikes, car accidents, predation, or other misadventure. In 2 cases, dull demeanor prevented a full neurologic assessment on admission, but demeanor improved rapidly when treated with meloxicam. The presence of additional neurologic deficits in most cases may be suggestive of central, or first-order, Horner syndrome, in which ataxia, postural-reaction deficits, altered mental status, and cranial nerve deficits are common. (17) Radiographs were obtained for all affected patients; however, further imaging such as computed tomography and magnetic resonance imaging are recommended to identify anatomic lesions, such as dissecting artery or neoplasia. (17,18)

Topical pharmacologic testing was not used in these cases but is recommended to confirm or localize Horner syndrome lesions. (12) Cocaine and hydroxyamphetamine are not readily available in Australia; however, phenylephrine has been used in birds and apraclonidine has been suggested as a more-accessible alternative. (5,19) Phenylephrine is a direct-acting sympathomimetic amine that allows localization of Horner syndrome lesions through denervation hypersensitivity. (20) Results can vary with the time delay from injury and the completeness of the lesion injury. (13) Future investigation would benefit from pharmacologic testing, especially when the time of injury is known, to better elucidate the underlying causes of Horner syndrome in wild birds.

A marked variation in outcome was observed between dosing regimens of meloxicam, with the dose of 1 mg/kg appearing more effective than 0.2 mg/kg for traumatic cases of Horner syndrome. The limited number of cases prevented statistical analysis but is warranted in future studies. It is clear, however, that Horner syndrome in wild birds confers a poor prognosis for recovery and is a significant finding of the neurologic exam. Resolution of clinical signs is variable and often prolonged in domestic mammals and birds. (3,21) Hospitalization times in wild birds were highly variable, and resolution was gradual. However, fatal cases treated with meloxicam at 1 mg/kg were more likely to decline rapidly in the first 4 days. Persistence of Horner syndrome beyond resolution of surrounding soft tissue trauma appears to be a common feature of Horner syndrome in birds and is consistent with previous reports. (5)

Further investigation of the underlying causes of Horner syndrome in birds and wider reporting of affected cases are necessary to provide prognostic guidelines and accurate recommendations for management and treatment.

Andrew G. Hill, BVSc, MVSc, MANZCVS (Avian)

From the Currumbin Wildlife Sanctuary. 28 Tomewin Street, Currumbin, QLD 4223, Australia.

References

(1.) Smith SJ, Diehl N, Leavitt JA, Mohney BG. Incidence of pediatric Horner syndrome and the risk of neuroblastoma: a population-based study. Arch Ophthalmol. 2010;128(3);324-329.

(2.) Kern TJ, Aromando MC, Erb HN. Horner's syndrome in dogs and cats: 100 cases (1975-1985). J Am Vet Med Assoc. 1989;195(3):369-373.

(3.) Gancz AY, Lee S, Higginson G, et al. Horner's syndrome in an eastern screech owl (Megascops asio). Vet Rec. 2006;159(10):320-322.

(4.) Williams DL, Cooper JE. Horner's syndrome in an African spotted eagle owl (Bubo africanus). Vet Rec. 1994;134(3):64-66.

(5.) Gancz AY, Malka S, Sandmeyer L, et al. Horner's syndrome in a red-bellied parrot (Poicephalus rufiventris). J Avian Med Surg. 2005; 19(1):30-34.

(6.) Isomura G. A nerve originating from the superior cervical ganglion in the fowl. Anat Anr. 1973; 133(1): 82-89.

(7.) Quay WB. Effects of melatonin implants on structures and behaviors of the house finch (Carpodacus mexicanus) eye. J Pineal Res. 1986;3(2): 143-157.

(8.) Bennett T, Burnstock G, Cobb JL. Malmfors T. An ultrastructural and histochemical study of the short-term effects of 6-hydroxydopamine on adrenergic nerves in the domestic fowl. Br J Pharmacol. 1970; 38(4):802 809.

(9.) Drenckhahn D, Jeikowski H. The myotendinous junction of the smooth feather muscles (mm. pennati): a light and electron microscopic study on a myoelastic system. Cell Tissue Res. 1978; 194(1); 151-162.

(10.) Aalbers MW, Rijkers K. Van Winden LA, et al. Horner's syndrome: a complication of experimental carotid artery surgery in rats. Auton Neurosci. 2009; 147(1-2):64-69.

(11.) Smith JS, Mayhew IG. Horner's syndrome in large animals. Cornell Vet. 1977;67(4):529-542.

(12.) Pilley SF, Thompson HS. Pupillary "dilatation lag" in Horner's syndrome. Br J Ophthalmol. 1975; 59(12):731-735.

(13.) De Risio L, McConnell JF. Second order Horner's syndrome in a cat .J Feline Med Surg. 2009; 11(8); 714-716.

(14.) Simpson KM, Williams DL, Cherubini GB. Neuropharmacological lesion localization in idiopathic Horner's syndrome in golden retrievers and dogs of other breeds. Vet Ophthalmol. 2015; 18(1): 1-5.

(15.) Bell RL, Atweh N, Ivy ME, Possenti P. Traumatic and iatrogenic Horner syndrome: case reports and review of the literature. J Trauma. 2001 ;51(2):400-404.

(16.) Boydell P. Horner's syndrome following cervical spinal surgery in the dog. J Small Anim Pract. 1995; 36(11):510-512.

(17.) Norris JW, Beletsky V, Nadareishvili ZG. Sudden neck movement and cervical artery dissection: the Canadian Stroke Consortium. Can Med Assoc J. 2000; 163(1):38 40.

(18.) Mahoney NR, Liu GT, Menacker SJ, et al. Pediatric Horner syndrome: etiologies and roles of imaging and urine studies to detect neuroblastoma and other responsible mass lesions. Am J Ophthalmol. 2006; 142(4):651-659.

(19.) Koc F, Kavuncu S, Kansu T, et al. The sensitivity and specificity of 0.5% apraclonidine in the diagnosis of oculosympathetic paresis. Br J Ophthalmol. 2005;89(11): 1442-1444.

(20.) Smith SA, Smith SE. Evidence for a neuropathic aetiology in the small pupil of diabetes mellitus. Br J Ophthalmol. 1983;67(2):89-93.

(21.) Morgan RV, Zanotti SW. Horner's syndrome in dogs and cats: 49 cases (1980-1986). J Am Vet Med Assoc. 1989; 194(8): 1096-1109.

Caption: Figure 1. Acquired Horner syndrome in a rainbow lorikeet with concurrent beak trauma. Unilateral denervation causes a clear central demarcation of feather erection in frontal (a) and oblique right (b) views. Ptosis and feather erection on the affected left side (c), creating asymmetry compared with unaffected right side (d).

Caption: Figure 2. Right-sided feather erection (open arrowhead) and right ptosis (black arrowhead) in an Australian magpie with Horner syndrome.
Table 1. Summary of clinical findings from 25 wild
birds with unilateral ptosis and facial feather erection
admitted to Currumbin Wildlife Hospital between 2010 and 2016.

Case No.   Spccies               Age        History

1          Rainbow lorikeet      Subadult   Unable to fly

2          Crested pigeon        Adult      Ground find

3          Torresian crow        Adult      Unknown

4          Laughing kookaburra   Adult      Vehicle impact

5          Crested tern          Subadult   Ground find

6          Rainbow lorikeet      Adult      Ground find

7          Southern boobook      Adult      Referred by
                                            caregiver

8          Rainbow lorikeet      Adult      Swimming
                                            pool incident

9          Rainbow lorikeet      Subadult   Unable to fly

10         Rainbow lorikeet      Adult      Unable to fly

11         Rainbow lorikeet      Adult      Vehicle impact

12         Scaly breasted        Adult      Ground find
           lorikeet

13         Rainbow lorikeet      Subadult   Window hit

14         Rainbow lorikeet      Adult      Window hit

15         Scaly breasted        Adult      Ground find
           lorikeet

16         Grey butcherbird      Subadult   Unknown

17         Tawny frogmouth       Adult      Ground find

18         Tawny frogmouth       Adult      Ground find

19         Rainbow lorikeet      Subadult   Ground find

20         Scaly breasted        Subadult   Window hit
           lorikeet

21         Rainbow lorikeet      Subadult   Unable to fly

22         Scaly breasted        Subadult   Unable to fly
           lorikeet

23         Rainbow lorikeet      Adult      Ground find

24         Rainbow lorikeet      Adult      Ground find

25         Rainbow lorikeet      Adult      Cat caught

Case No.   Spccies               Demeanor   Additional injuries

1          Rainbow lorikeet      Quiet      None

2          Crested pigeon        Quiet      Coracoid and
                                            clavicle fractures

3          Torresian crow        Quiet      None

4          Laughing kookaburra   Normal     Keel fracture.
                                            palate bruising

5          Crested tern          Quiet      None

6          Rainbow lorikeet      Normal     Left wing drop

7          Southern boobook      Normal     Corneal ulcer,
                                            pectin rupture

8          Rainbow lorikeet      Normal     Beak fracture

9          Rainbow lorikeet      Normal     None

10         Rainbow lorikeet      Normal     Beak fracture,
                                            superficial head
                                            trauma

11         Rainbow lorikeet      Quiet      Respiratory
                                            hemorrhage

12         Scaly breasted        Quiet      None
           lorikeet

13         Rainbow lorikeet      Quiet      Beak fracture

14         Rainbow lorikeet      Normal     None

15         Scaly breasted        Normal     None
           lorikeet

16         Grey butcherbird      Normal     None

17         Tawny frogmouth       Quiet      Corneal trauma

18         Tawny frogmouth       Normal     None

19         Rainbow lorikeet      Quiet      Beak trauma

20         Scaly breasted        Quiet      Beak trauma
           lorikeet

21         Rainbow lorikeet      Quiet      None

22         Scaly breasted        Quiet      PBFD feather loss
           lorikeet

23         Rainbow lorikeet      Quiet      None

24         Rainbow lorikeet      Normal     Beak injury, dyspnea

25         Rainbow lorikeet      Quiet      PBFD feather loss

Abbreviation: PBFD indicates psittacine beak and feather disease.

Table 1. Extended.

Horner          Other neurologic signs
syndrome side

Right           Ataxia

Left            Loss of tail flick reflex

Not recorded    Ataxia

Left            Nystagmus and loss
                of corneal reflex

Left            None

Right           Ataxia

Right           None

Right           Loss of tail flick reflex

Right           None

Left            Hindlimb paralysis and loss
                of tail flick reflex

Not recorded    Hindlimb paralysis

Left            Hindlimb paralysis

Left            None

Right           Hindlimb paresis and loss
                of tail flick reflex

Not recorded    None

Right           Head tilt to right

Left            Left wing paresis

Left            Anisocoria and tongue deviation to left

Not recorded    Hindlimb paresis

Not recorded    Hindlimb paresis

Not recorded    Ataxia

Not recorded    None

Left            Loss of corneal reflex, hindlimb
                paralysis, and loss of tail flick
                reflex

Left            Hindlimb paralysis and loss of
                tail flick reflex

Right           Hindlimb paresis and voice change

Horner             Stay      Outcome
syndrome side   length, hr

Right              102       Died or euthanatized

Left                24       Died or euthanatized

Not recorded        42       Died or euthanatized

Left                97       Died or euthanatized

Left                39       Died or euthanatized

Right               24       Died or euthanatized

Right               54       Died or euthanatized

Right              1557      Released

Right               75       Released

Left               161       Released

Not recorded        25       Died or euthanatized

Left                0        Died or euthanatized

Left               167       Released

Right              1867      Released

Not recorded       166       Released

Right               1        Died or euthanatized

Left                3        Died or euthanatized

Left                68       Released

Not recorded        29       Died or euthanatized

Not recorded        73

Not recorded        96       Died or euthanatized

Not recorded        0        Died or euthanatized

Left                16       Died or euthanatized

Left                2        Died or euthanatized

Right               3        Died or euthanatized

Table 2. Species and survival of 25 wild birds presented
to Currumbin Wildlife Hospital with Horner syndrome
between 2010 and 2016.

                           Affected,   Survival.
Species                     No. (%)     No. (%)

Rainbow lorikeet            13 (52)      5 (38)
Scaly breasted lorikeet      4 (16)      2 (50)
Tawny frogmouth              2 (8)       1 (50)
Laughing kookaburra          1 (4)       0 (0)
Southern boobook             1 (4)       0 (0)
Crested pigeon               1 (4)       0 (0)
Crested tern                 1 (4)       0 (0)
Grey butcherbird             1 (4)       0 (0)
Torresian crow               1 (4)       0 (0)

Table 3. Concurrent neurologic deficits observed in 25
wild birds with unilateral Horner syndrome.

                              Birds affected.
Neurologic deficit                No. (%)

Hindlimb paralysis/paresis         9 (36)
Loss of tail flick reflex          6 (24)
Ataxia                             4 (16)
Loss of corneal reflex             2 (8)
Voice change                       1 (4)
Wing paresis                       1 (4)
Anisocoria                         1 (4)
Head tilt                          1 (4)
Nystagmus                          1 (4)
Asymmetry of tongue                1 (4)
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Title Annotation:Retrospective Study
Author:Hill, Andrew G.
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Geographic Code:8AUST
Date:Jun 1, 2018
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