Introduction
Blunt force trauma is a significant cause of morbidity and mortality in raptorial species, with collisions into anthropogenic structures (vehicles, windows, wind turbines, buildings, and power lines) being the most common cause.1–6 Head trauma is a common component of blunt force trauma, and severe head trauma is associated with high mortality.7–10 As vehicular collisions are a common cause of blunt force trauma in free-living wildlife, head trauma is understandably a common presenting condition.4,6,11 Clinical signs of head trauma in avian species include alterations in mentation; ocular changes (detached retina, blood in the anterior chamber or vitreous, lens luxation, and iridial tears); presence of blood in the ears, nares, or mouth; and facial trauma (soft tissue and orthopedic).12–15 While there are published recommendations for diagnosis and treating head trauma in dogs and cats,16–20 as well as in humans,8,21–24 only limited resources exist for avian equivalents.25–27 Treatment in these animals is often based on comparisons with small animal medicine and anecdotal experience.
The Glasgow Coma Scale (GCS) is an objective evaluation of the level of consciousness in human patients by assessing motor, verbal, and eye responses graded on respective scales of 4, 5, and 6.28 These 3 components can then be scored separately or combined for a total score, ranging from 3 to 15.28–30 Studies have demonstrated a positive linear relationship between the sum scores and mortality in head trauma patients.29,31 These studies correlated the severity of trauma based on the total GCS with prognosis as follows: mild (> 12), moderate (9 to 12), and severe (< 9).31 This scale had been modified for use in veterinary medicine, enabling grading of the initial neurologic status and serial monitoring. This Modified GCS (MCGS) also evaluates 3 components of neurologic function: motor activity, brain stem reflexes, and level of consciousness.30,32 Similar to human studies, the probability of survival in head trauma dogs is linear and positively correlated with the MGCS score, with total scores ranging from 3 to 8 associated with a grave prognosis, 9 to 14 associated with a guarded prognosis, and 15 to 18 associated with a good prognosis.7,32
While the GCS is used widely, questions remain regarding its reliability and accuracy based on the user’s skill set.28,33 Despite these concerns, the GCS is still used heavily in human medicine as a prognostic indicator for head trauma.8,24,28,34 This inconsistency in user evaluation needs to be considered and reduced before utilizing a similar scoring system in an animal care practice. Additionally, the accuracy and reliability of the MGCS has to be evaluated in veterinary medicine. As there are usually a variety of training levels within facilities, both in veterinary hospitals and wildlife rehabilitation centers, an unreliable prognostic tool between individuals would not be practical. Most rehabilitation facilities are not-for-profit, so the economical use of funds is critical. Any tool that can improve triage management can save time, resources, and labor or help guide alterations to treatment protocols to improve survival. A reliable means of assessment will also lead to improved animal welfare.
The aims of this prospective multi-institutional study were 2-fold. The first aim was to develop an avian-specific MGCS for use in raptors presenting with head trauma and assess the agreement of the MGCS scores between examiners with varying backgrounds (veterinary students, wildlife rehabilitation veterinarians, and veterinary neurologists). The second aim was to assess the prognostic value of the avian MGCS in raptors with head trauma. We hypothesized that the avian MGCS would be comparable across examiners and that the avian MCGS would be correlated to survival at 48 hours. As based on the literature in human and veterinary medicine, we predicted that scores ≤ 8 would have a higher mortality rate than those with a score > 8.
Methods
Development of an avian Modified Glasgow Coma Scale
The authors developed an avian MGCS based on a previously established MGCS utilized in canine patients.32,35 Adjustments were made to the canine MGCS to account for raptor bipedalism and the presence of wings. To make the scale as objective as possible, precise language was also utilized. Similar to the human GCS and the canine MGCS, this scale targeted 3 components of neurologic function, each scored from 1 to 5: motor activity, level of consciousness, and brain stem reflexes (Supplementary Material S1).
Animals
This multi-institutional prospective study included native raptor species presenting to the University of Illinois Wildlife Medical Clinic (Urbana, Illinois), The Raptor Center at the University of Minnesota (Saint Paul, Minnesota), and the Carolina Raptor Center (Huntersville, North Carolina) with a known history of head trauma or with physical examination findings indicative of head trauma from January 1, 2018, to December 31, 2019. Physical examination findings consistent with head trauma included ocular changes (detached retina, hyphema, and vitreal hemorrhage), blood or bruising in the ears/nares/mouth, and facial/beak/skull fractures. Patients were excluded if they were euthanized within the first 48 hours after admission due to severe, concurrent disease unrelated to head trauma, such as open, comminuted, or articular fractures, or if there was the presence or suspicion of a coagulopathy.
User agreement of an avian Modified Glasgow Coma Scale
All raptors meeting the inclusion criteria presenting to the University of Illinois Wildlife Medical Clinic received an avian MGCS assessment performed by 3 separate individuals within 8 hours of presentation: a student volunteer, a wildlife rehabilitation veterinarian, and a board-certified veterinary neurologist or resident in veterinary neurology, with each evaluator blinded to the scores of the other evaluators. Descriptive statistics for each component associated with an overall coma score were tabulated for each rater, including median and minimum-maximum. The intrarater agreement was assessed in 2 ways: (1) Cronbach α and (2) intraclass correlation. All statistical analyses were performed using commercial software (MedCalc version 16; MedCalc Software Ltd).
Prognostic value of an avian Modified Glasgow Coma Scale
All raptors presenting to each of the 3 institutions meeting the inclusion criteria had an avian MGCS performed by a veterinarian within 8 hours of presentation. Additional information collected included species, sex (when determination was possible), age (juvenile, adult, or unknown), and survival status (survivor or nonsurvivor) at 48 hours postadmission.
Univariate associations comparing demographic factors and the MGCS determined by a wildlife rehabilitation member at each institution were determined using a Fisher exact test. Differences in scores for neurologic examination components and overall scores for individual birds were tested using the Kruskal-Wallis test. Statistical significance was set at P < .05 for all analyses performed.
Results
Animals
A total of 156 raptors representing 16 native North American species were enrolled. Of those, 19 (12.2%) were from the University of Illinois Wildlife Medical Clinic, 55 (35.3%) were from The Raptor Center at the University of Minnesota, and 82 (60.3%) were from the Carolina Raptor Center. There were 86 nocturnal and 70 diurnal species. Specific species included the barred owl (Strix varia; 60/156 [38.5%]), Cooper’s hawk (Accipiter cooperii; 23/156 [14.7%]), red-tailed hawk (Buteo jamaicensis; 21/156 [13.5%]), great horned owl (Bubo virginianus; 13/156 [8.3%]), red-shouldered hawk (Buteo lineatus; 9/156 [5.8%]), eastern screech owl (Megascops asio; 7/156 [4.5%]), bald eagle (Haliaeetus leucocephalus; 7/156 [4.5%]), northern saw-whet owl (Aegolius acadicus; 5/156 [3.2%]), broad-winged hawk (Buteo platypterus; 4/156 [2.6%]), and 1 of 156 (0.6%) of each of the following: snowy owl (Bubo scandiacus), sharp-shinned hawk (Accipiter striatus), peregrine falcon (Falco peregrinus), barn owl (Tyto alba), turkey vulture (Cathartes aura), American kestrel (Falco sparverius), and unknown. Patients were recorded as juvenile (61/156 [39.1%]), adult (75/156 [48.1%]), or of unknown/not recorded age (20/156 [12.8%]). Patients were categorized as unable to be sexed (98/156 [62.8%]) male (30/156 [19.2%]), or female (28/156 [17.9%]).
Avian MCGS
The avian MGCS was developed with 3 assessment components (motor activity, level of consciousness, and brain stem reflexes), each with a scale from 1 to 5, creating a score ranging from 3 to 15 (Supplementary Material S1). Individual avian MGCS component scores and total scores are reported for each species (Table 1). Thirty-one of 156 (19.9%) birds received a total score of < 8, while 125/156 (80.1%) had a total score of > 8.
Avian Modified Glasgow Coma Scale scores and survival rates at 48 hours for 156 raptors presenting to rehabilitation centers between January 1, 2018, and December 31, 2019.
Species | Motor | Level of consciousness | Brain stem | Total MGCS | No. (%) survived |
---|---|---|---|---|---|
Barred owl (Strix varia; n = 60) | 4 (1–5) | 4 (2–5) | 2 (1–5) | 11 (5–15) | 19 (31.7%) |
Great horned owl (Bubo virginianus; n = 13) | 4 (1–5) | 4 (2–5) | 4 (1–5) | 12 (6–15) | 6 (46.2%) |
Eastern screech owl (Megascops asio; n = 7) | 4 (1–5) | 3 (3–5) | 5 (1–5) | 11 (6–15) | 4 (57.1%) |
Saw-whet owl (Aegolius acadicus; n = 5) | 5 (3–5) | 5 (4–5) | 5 (4–5) | 14 (13–15) | 4 (80%) |
Barn owl (Tyto alba; n = 1) | 5 | 4 | 5 | 14 | 1 (100%) |
Snowy owl (Bubo scandiacus; n = 1) | 2 | 3 | 5 | 10 | 1 (100%) |
Cooper’s hawk (Accipiter cooperii; n = 23) | 4 (1–5) | 4 (2–5) | 5 (1–5) | 12 (6–15) | 12 (52.2%) |
Red-tailed hawk (Buteo jamaicensis; n = 21) | 4 (2–5) | 4 (3–5) | 4 (1–5) | 12 (7–15) | 11 (52.4%) |
Bald eagle (Haliaeetus leucocephalus; n= 7) | 4 (2–5) | 4 (2–5) | 5 (2–5) | 11 (9–14) | 4 (57.1%) |
Broad-winged hawk (Buteo platypterus; n = 4) | 4 (3–5) | 4.5 (4–5) | 4.5 (2–5) | 12 (11–15) | 2 (50%) |
Sharp-shinned hawk (Accipiter striatus; n = 1) | 2 | 4 | 2 | 8 | 0 (0%) |
Turkey vulture (Cathartes aura; n = 1) | 3 | 3 | 1 | 7 | 0 (0%) |
Unknown (n = 1) | 4 | 4 | 4 | 12 | 0 (0%) |
All birds (n = 156) | 4 (1–5) | 4 (2–5) | 4 (1–5) | 12 (5–15) | 73 (46.8%) |
User agreement
User agreement was assessed for 19 birds. There was excellent agreement between all 3 raters for the assessment of motor activity (α = 0.9185), brain stem reflex (α = 0.9153), and overall score (α = 0.962) and good agreement for assessing the level of consciousness (α = 0.8319). There was good correlation between the 3 raters for assessment of motor activity (0.9042; 95% CI, 0.77 to 0.96), loss of consciousness (0.8300; 95% CI, 0.62 to 0.94), brain stem activity (0.7838; 95% CI, 0.58 to 0.91, and overall score (0.9453; 95% CI, 0.84 to 0.98). The 3 raters had considerable overlap in scores for all categories (Figure 1).
Box-and-whisker plots of avian Glasgow Coma Scale scores by 3 raters for motor activity (A), loss of consciousness (B), brain stem reflex (C), and overall score (D) for 156 raptors presenting to rehabilitation centers between January 1, 2018, and December 31, 2019. For each plot, the box represents the IQR (25% to 75%) and the line within each box delineates the median value. There was good correlation between the 3 raters for assessment of motor activity (0.9042; 95% CI, 0.77 to 0.96) and overall score (0.9453; 95% CI, 0.84 to 0.98). There was good correlation in the assessment of loss of consciousness (0.8300; 95% CI, 0.62 to 0.94) and brain stem activity (0.7838; 95% CI, 0.58 to 0.91). There is considerable overlap among all raters in scores for all categories.
Citation: Journal of the American Veterinary Medical Association 261, 11; 10.2460/javma.23.05.0225
Prognostic value
Seventy-three out of 156 (46.8%) raptors were alive at 48 hours, while 83 (53.2%) were not. Of the raptors with a total MGCS score ≤ 8, only 4 of 31 (12.9%) survived up to 48 hours, whereas 69 of 125 (55.2%) raptors with a total score > 8 survived (Table 2).
Avian Modified Glasgow Coma Scale scores and 48-hour survival statistics for 156 raptors presenting to rehabilitation centers in North America between January 1, 2018, and December 31, 2019.
Total avian MGCS | Total No. of raptors | Survival (%) |
---|---|---|
5 | 2 | 0 (0%) |
6 | 5 | 1 (20%) |
7 | 12 | 1 (8.3%) |
8 | 12 | 2 (16.7%) |
9 | 19 | 5 (26.3%) |
10 | 7 | 3 (42.8%) |
11 | 20 | 8 (40%) |
12 | 22 | 12 (54.5%) |
13 | 16 | 8 (50%) |
14 | 24 | 20 (83.3%) |
15 | 17 | 13 (76.5%) |
Variables that were associated with higher survival rates in the univariate analysis included the treating institution (χ2 = 9.441; P = .009), higher motor activity scores (P = .003), level of consciousness scores (P = .002), brain stem reflex scores (P < .0001), and total avian MGCS scores (P < .0001; Figure 2). There was no significant difference in survival between species (χ2 = 11.846; P = .106) or sex (χ2 = 2.690; P = .261). However, diurnal birds (51/83 [63%]) were more likely to survive than nocturnal birds (30/68 [44%]; P = .016). There was no significant difference in total avian MGCS score between diurnal (median, 12; min/max, 6 to 15) and nocturnal (median, 11; min/max, 5 to 15) species (P = .08). There was a difference in score for level of consciousness (P = .001) between age classes but not motor activity (P = .226), brain stem reflex (P = .826), or total neurologic score (P = .132). There was no difference in score between sexes for motor activity (P = .989), level of consciousness (P = .545), brain stem reflex (P = .051), or total neurologic score (P = .253).
Box-and-whisker plots for 48-hour survival statistics for the raptors described in Figure 1, grouped by their avian Glasgow Coma Scale score for motor activity (A), brain stem reflexes (B), level of consciousness (C), or overall score (D). For each plot, the box represents the IQR (25% to 75%) and the line within each box delineates the median value. *P < .05; birds with higher scores for motor activity, brain stem reflexes, level of consciousness, and total score were more likely to remain alive at 48 hours postpresentation to rehabilitation centers.
Citation: Journal of the American Veterinary Medical Association 261, 11; 10.2460/javma.23.05.0225
Discussion
The first aim of this study was to assess the agreement of the MGCS scores assigned to raptors between examiners with varying backgrounds. In this study, an avian-specific MGCS was developed and applied to raptors presenting with head trauma. For the cohort of raptors that had serial assessments, the MGCS demonstrated good-excellent agreement among raters of various backgrounds. When using the avian-specific MGCS, there was excellent agreement among all raters in regard to assessing motor activity, brain stem reflexes, and the overall score and good agreement for assessing level of consciousness. Additionally, there was considerable overlap in all categories between all raters, regardless of experience. In human medicine, the GCS is the best indicator for evaluating prognosis on the basis of its simplicity, the fact that it is less time-consuming, and its effectiveness in the emergency department (ED).36,37 However, the reliability of the GCS is of debate. While this scale is highly used and shown to have interobserver reliability when performed by trained medical personnel, the reliability needs to be improved in clinical practice when performed by those less trained in this assessment.28,29,31,36,38 A study by Jeffery et al36 showed inconsistencies in the knowledge of the GCS and its application among staff in a human orthopedics department, and intervention with a single teaching session improved these deficiencies. This could indeed be the case for the findings in this study. As the assessment of user agreement was performed at only 1 institution, all individuals participating in the study had training on how to perform an avian neurologic examination, which could have improved the accuracy of patient assessment within the institution. Future multi-institutional studies assessing interobserver reliability are warranted and may consider including technicians, as they are valued parts of the veterinary health-care team.
The second aim was to assess the prognostic value of the avian MGCS in raptors with head trauma. We hypothesized that raptors presenting with a GCS ≤ 8 would have a higher mortality rate than those with a score > 8. Indeed, this study demonstrated that animals with higher scores in each of the individual categories and the overall score had a higher likelihood of survival. More specifically, animals with a total score of > 12 were more likely to survive and those with a total score of < 10 were unlikely to survive. These findings are similar to what is reported in humans and canines. In humans, the GCS score is linearly related to poor outcomes if it is in the range of 3 to 9 within the first 24 hours,39–41 and in dogs, lower scores are associated with a higher mortality rate and a < 50% chance of survival in 72 hours.32 To date, there are few studies in a nonhuman species (canines) investigating the prognostic utility of the MGCS.32,42 There are no prospective or retrospective studies investigating its accuracy or reliability. Our data did show a difference in brain stem reflexes and total neurologic scores among institutions. Although each institution’s inclusion and exclusion criteria were similar, the case presentations and patient care protocols may have varied, potentially impacting case outcomes. This study shows that the avian-specific MGCS may be correlated with the probability of survival within the first 48 hours after presentation to rehabilitation facilities in raptors with head trauma.
Assessment of brain stem reflexes presents a challenge in assessing the avian MGCS due to the frequent presence of concurrent ocular trauma in raptors with head trauma. Ocular lesions are frequently associated with traumatic brain injury (TBI) in raptors because the orbit takes up a large proportion of the skull.43 Many examination parameters used to assess brain stem reflexes depend on the external assessment of ocular structures (pupillary constriction, pupil size, etc). Therefore, any concurrent ocular trauma affecting the assessment of the brain stem reflexes could, by default, give the patient a lower score. Evaluation of physiologic nystagmus can be complex in healthy raptors, as there are reduced extraocular muscles; therefore, this test requires complete head movement.43 In a patient suffering from trauma, excessive movement may be limited or not recommended, thus making it difficult to assess or reflect a falsely lower score. Similar challenges are noted in canine medicine. Accurate scoring is difficult in specific scenarios, such as in patients with eyelid swelling, mature cataracts, late-stage keratoconjunctivitis sicca, retinal detachment, glaucoma, or eyeball loss.44
Another issue when assessing brain stem reflexes is the pupillary light reflex evaluation. Unlike mammals, the iris sphincter muscles are mainly striated skeletal muscles.45 Similar to other animals, light-driven changes to the pupil in birds are still somewhat related to the illumination level, with the sensitivity also being dependent on species and age. Diurnal birds may require more light for pupil constriction than nocturnal species, as their retina is less sensitive and requires higher light levels for photo capture. Additionally, the pupillary light reflex of most birds is relatively modest compared to that of mammals. For example, the pupils of owls only constrict up to 30% of their dark-adapted area versus mammals, which will contract to just a few percent of the fully dilated pupil in bright light.45 Therefore, it is possible that some birds were over or underscored in this specific assessment. However, no differences were found in total avian MGCS score between diurnal and nocturnal species. Diurnal birds were found to be more likely to survive past 48 hours than nocturnal birds. One speculation for this finding may be that diurnal birds are active during the day, and therefore their injuries would also occur during this time. It is possible that due to this, the diurnal species may have been found and presented sooner than the nocturnal species.
The score for level of consciousness was found to be higher in adult raptors compared to juveniles. Interestingly, in humans, some studies have shown that elderly patients with TBI have higher GCS scores than younger patients with similar TBI severity.46 An explanation for this finding is that elderly patients have a blunted or delayed clinical response to injury compared with younger patients. This blunted response could be due to differences in the physiologic response to injury between younger and older patients, including a decreased inflammatory response to injury, differences in vasoreactivity and brain swelling, or a decreased extent of neuroexcitatory depolarization after brain injury, among other possible differences.46 Certainly, there are species differences, which may not be accurate in raptors. Additionally, the exact age of our raptor patients was unknown; for this study, the patients were listed simply as juvenile versus adult, which can be highly subjective.
This study was not without limitations. For instance, the order of assessment category was not randomized and only a single assessment was performed to determine the score, which has been shown to be unreliable in human medicine.47 Serial assessments are recommended to detect any change in a patient’s neurologic status, which could indicate new or evolving brain injury requiring emergent attention.47,48 The reason for performing a single assessment in this study was to avoid excessive handling of these wild animals, which could be detrimental to their conditions. Another limitation was that patient assessments were within the first 8 hours of presentation, so there was potential for their scores to have changed significantly (ie, a patient with an initially higher score could have deteriorated and not survived, etc). Therefore, these possible changes between examinations may have impacted the assessment of user agreement. However, we would expect that if the neurologic status changed significantly, there would not likely be significant agreement. Additionally, as these were wild animals, the time frame from the injury to presentation was also unknown. In humans, prehospital GCSs are shown to be different from those scores upon arrival to the ED.49 In 1 study50 assessing agreement between prehospital and ED GCS, patients were classified on the basis of their scores: 13 to 15 was mild, 9 to 12 was moderate, and 3 to 8 severe.The study found that for patients classified as having moderate to severe TBI, agreement was low between prehospital and ED GCSs.50 However, inter-rater variability could also not be excluded.
The scale used in this study was based on category scores ranging from 1 to 5, with a total score ranging from 3 to 15. This differs from what has been used in veterinary medicine, with categorical scores ranging from 1 to 6 and a possible total score of 3 to 18. For the purpose of this study, the MGCS used in veterinary medicine was further modified to be utilized in avian species. As such, some of the tests performed in the canine were either not able to be performed safely in the patients or findings carried significant overlap. These modifications were made so that the scale would be as user-friendly as possible. With this being said, the different ranges in this scale may make its application and interpretation more difficult for clinicians more familiar with the MGCS used in the canine.
Another limitation, as stated above, was that the assessment of interobserver agreement was performed at only 1 institution. All individuals participating in the study at this institution were provided training on performing an avian neurologic examination, which likely improved interobserver agreement. However, none of the raters were trained in utilizing the avian-specific MGCS, so the study may truly reflect that individuals with varying backgrounds can utilize this rating system. Lastly, the outcome was assessed 48 hours after admission and did not consider the possibility of death after this time frame. For the study, 48 hours was elected, as many rehabilitation facilities must make triage and treatment decisions for patients in a short time due to funding and facility factors.
Additionally, our only outcome measure was life or death and we did not consider functional capacity. One reason is that this can be very difficult to quantify in animal patients statistically,32 and more importantly, these are wild animals, and their survival in the wild is ultimately dependent on their functional capacity. Therefore, if they cannot safely be rereleased, human euthanasia is often elected. Lastly, we could not confirm TBI as the cause of the birds’ signs in all cases. While the inclusion criteria were made to avoid enrolling birds whose signs were not due to trauma, without confirmation via necropsy, it is still possible that birds suffering from other conditions may have been enrolled. It is also possible that even in birds with head trauma, underlying comorbidities, such as additional trauma to internal organs or other preexisting comorbidities, may have impacted their survival and the cause of death was not directly due to their TBI.
In conclusion, we were able to develop and apply an avian-specific MGCS in the assessment of raptors with head trauma. This avian-specific MGCS overall showed good agreement amid raters with various backgrounds. Additionally, when used for prognostic purposes, raptor patients with an avian MGCS of < 10 were found to have a lower chance of survival.
Acknowledgments
None reported.
Disclosures
Portions of this study were presented at the American Association of Zoo Veterinarians Annual Conference, Saint Louis, Missouri, 2019.
No AI-assisted technologies were used in the generation of this manuscript.
Funding
The authors have nothing to disclose.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org
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