Fracture Analysis of Wild Birds in South Korea

pISSN 1598-298X / eISSN 2384-0749 J Vet Clin 36(4) : 196-199 (2019) http://dx.doi.org/10.17555/jvc.2019.08.36.4.196

Hyun-Kyu Jang, Jong-Moon Park, Sohail Ahmed, Seong-Hoon Seok*, Ho-Su Kim** and Seong-Chan Yeon1 Department of Veterinary Clinical Sciences and Research Institute for Veterinary Science, Seoul Wildlife Center, College of Veterinary Medicine, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, Korea *Daegu Animal Medical Center, 36, Dongdaegu-ro, Suseong-gu, Daegu 42185, Korea **Busan Wildlife Treatment Center, 1240-2, Nakdongnam-ro, Saha-gu, Busan 49435, Korea

(Received: April 05, 2019 / Accepted: August 10, 2019)

Abstract : This study was conducted to evaluate and analyze fractures types, sites and surgical approach of wild birds in Korea. The study was conducted on data collected for fracture lesion sites, species, outcomes, surgical methods, treatments and medical records from wildlife centers in South Korea. All birds were subjected to clinical examination, followed by surgical invasion and post-operative care. Fractures were more common in adult non-raptor species (51.57%) as compared to raptors (48.43%). Of the 254 cases evaluated, maximum cases comprised ulnar fractures (29.70%), followed by radial (21.76%) and humeral fractures (17.35%). Treatment procedures at 340 fracture sites were maximally treated with figure-8 bandage (33.07%), external skeletal fixator-intramedullary pin (ESF+IM tie-in fixation) (20.86%), and other varied procedures. All birds were kept indoors till recovery. Treatment outcomes were dependent on the type of bone fractured and surgical method applied. Based on the surgical treatments and outcomes, birds were kept hospitalized, and released or euthanized. The findings of this study provide information for veterinarians regarding the fractures sites, basic database for the species and outcomes of fracture repair in wild birds. Key words : birds, raptors, fracture repair, figure-8 bandage, wildlife.

Introduction and incorporate non-invasive surgical techniques for wild birds (5). To select an appropriate and adaptable technique, A number of practical considerations need to be accounted data was collected from 3 wildlife centers. We evaluated site for with wildlife than with domestic animals. Since wildlife and type of fractures, distribution of fracture sites according have no owner to provide financial support for their needs, to the species, and outcomes of fracture managements. veterinarians who provide surgical care for wildlife have to Few studies have described and reported types of fractures also consider the post-operative care (9). Avian orthopedic in wildlife (14,15). The current study aimed to evaluate the techniques vary from mammalian procedures in several types of fractures in raptors and non-raptors, to assess the ways. Avian bones are thinner, more brittle, and pneuma- prevalence of fracture by considering the bone involved, and tized which are connected to air sacs (4). Because of these to help veterinarians in identifying treatment methods avail- reasons, many fractured avian bones tend to be comminuted able with their outcomes. and open fractures (11). These fractures are found in multiple bones such as the humerus, femur, radius, and ulna; Materials and Methods often, these are complex fractures consisting of multiple bones of the joint (2). We collected bird fracture data from Seoul, Gyeongnam, Numerous wild migratory birds exist in South Korea. Every and Busan wildlife centers, for the period February 2016 to year, a dozen to hundreds of birds are accepted in wildlife November 2018. Totally, 254 birds with 340 fracture sites centers presenting with bone fractures (6). Cage rest, cast and that received surgical correction were evaluated in this study. stent are frequently used for light injuries. In case of severe The collected data include species, number of cases, fracture injuries, internal and external fixation are recommended (1,3). lesion, treatment, and outcome of surgical invasion. As a wild bird has weaker bone strength compared to mam- The investigation was based on patient records maintained mals, and numerous vessels exist in the bone lacuna, frac- at the wildlife centers. Data was categorized according to the tures may prove to be much more critical and mortal for birds bones involved, i.e., skull, hind limbs, forelimbs, fused verte- (13). Since wild avians are more vulnerable to injury and an brae, and joints of birds. Details of data retrieved were arranged insanitary environment, even simple wounds can prove be in order of skull, coracoid, scapula, clavicle, humerus, radius, life threatening. Fortunately, clinicians are trying to develop ulna, femur, carpometacarpus, tarsometatarsus, tibiotarsus, digit, notarium and synsacrum. Considering the age, all fractures were categorized into 2 groups: juvenile and adults. 1Corresponding author. Surgical techniques or methods used to repair fracture and E-mail : [email protected] the prognosis of surgeries were evaluated considering their

196 Fracture Analysis of Wild Birds in South Korea 197 relevant outcomes, i.e., union, non-union, malunion, osteo- tiple fractures were also investigated; these include the notar- myelitis, appliance failure, and amputation of affected body ium, synsacrum and skull (0.29% each), as presented in part of the bird. Table 2. Ventrodorsal radiograph of comminuted left radial Different surgical treatments were implemented; these and ulnar fractures are shown in Fig 4A and 4B. include figure-8 bandage, IM pinning, ESF + IM pin (tie-in fixation), splint, interdigital bandage, and ball bandage. Age and taxonomy Depending on the type of surgical invasion, site of fracture, Broadly, there are two categories with respect to age: juve- and outcome of treatments, the birds were categorized as nile and adult birds. Fracture percentage was greater in adults hospitalized, euthanized, death during hospitalization and (88.18%) as compared to juvenile birds (8.82%). surgery, or reintroduced into wild habitat. All records were Taxonomy of birds is widely differentiated in 2 categories: maintained according to the aim of the study. raptors and non-raptor species. The percentage of fracture in non-raptor species (51.57%) was higher than raptors (48.43%). Results Surgical methods for treatment Species distribution Different surgical methods are employed to treat fractures From data collected at the wildlife centers, 254 cases com- in birds. These include ball bandage, cage rest, digit ban- prising 60 different species underwent surgical repair of bone dage, figure-8 bandage, IM pin, ESF + IM pin (Fig 2A, 2B), fractures. Considering the species, Common kestrel (Falco splint, and tape splint. Treatments for the 254 birds evalu- tinnunculus) were the maximum (Fig 1A), followed by ated include cage rest, figure-8 bandage, IM pinning, ESF + Northern boobook (Ninox scutulata); distribution of the most IM pinning, splint, tape splint, interdigital bandage, and ball abundant species is given in Table 1. bandage. Of these, the figure-8 bandage was mostly fre-

Location of fracture Table 1. Most abundant species with different bone fractures According to the data, most fractures sites were related to treated at wildlife centers the forelimbs (ulna 29.70%, radius 21.76%, humerus 17.35%; Number Fig 1B), followed by tibiotarsus (8.82%), coracoid (7.05%), Common name Scientific name of cases carpometacarpus (5%; Fig 3A, 3B), femur (3.52%), and other rare cases of fractures in digits, coracoid, scapula and tar- Common kestrel Falco tinnunculus 40 sometatarsus. Pictorial representation of a humeral fracture Northern boobook Ninox japonica 22 prior to surgery is shown in Fig 1B. A few cases having mul- Eurasian sparrow hawk Accipiter nisus 17 Brown-eared bulbul Hypsipetes amaurotis 14 Rock dove Columba livia 13 Cinereous vulture Aegypius monachus 10 Common buzzard Buteo buteo 09 Large-billed crow Corvus macrorhynchos 08 Eurasian eagle owl Bubo bubo 08 Grey heron Ardea cinerea 06 Great egret Ardea alba 06 Eurasian hobby Falco subbuteo 05

Table 2. Location of fracture Location of fracture No. of patient affected Percentage Skull 001 000.29% Coracoid 024 007.05% Scapula 005 001.47% Clavicle 004 001.17% Humerus 059 017.35% Radius 074 021.76% Ulna 101 029.70% Carpometacarpus 017 005% Femur 012 003.52% Tibiotarsus 030 008.82% Tarsometatarsus 005 001.47% Digit 006 001.76% Fig 1. Common Kestrel (Falco tinnunculus). (A) Picture of wild Common Kestrel (Falco tinnunculus). (B) Common Kestrel Notarium 001 000.29% (Falco tinnunculus) with fractured left humerus prior to surgical Synsacrum 001 000.29% invasion at the wildlife center. Total 340 100% 198 Hyun-Kyu Jang, Jong-Moon Park, Sohail Ahmed, Seong-Hoon Seok, Ho-Su Kim and Seong-Chan Yeon

Fig 2. Humeral fracture in Common Kestrel (Falco tinnuncu- Fig 4. Radial and ulnar fractures. (A) Ventrodorsal radiograph of lus). (A) Post-operative picture of bird showing surgical repair Northern Boobook (Ninox japonica), revealing comminuted left of left humeral fracture with tie-in fixation using ESF + IM pin. radial and ulnar fractures. (B) Ventrodorsal radiograph of Little (B) Ventrodorsal radiograph showing surgical repair of the left Egret (Egretta garzetta), revealing comminuted left radial and humeral fracture with tie-in fixation using ESF + IM pin. ulnar fractures.

Table 3. Treatment of fracture Treatment No. of cases Percentage Cage rest 046 018.11% Figure-8 bandage 084 033.07% IM pinning 053 020.86% IM pin + ESF (tie in) 053 020.86% Splint 003 001.18% Tape splint 011 004.33% Interdigital bandage 003 001.18% Ball bandage 001 000.39% Total 254 100%

Table 4. Outcome during and after treatment Outcome No. of cases Percentage DOA 003 001.81% Hospitalized 013 005.12% Released 081 031.89% Euthanized 029 011.41% Dead 123 048.42% Pending 005 001.96% Total 254 100%

Fig 3. Carpometacarpal fracture in Common Kestrel (Falco tin- quently applied in 84 cases (33.07%). IM pinning and ESF + nunculus). (A) Ventrodorsal radiograph revealing comminuted IM pin followed with 53 cases (20.86% each). Other treat- left carpometacarpal fracture. (B) Ventrodorsal radiograph show- ment protocols were cage rest 46 (18.11%), tape splint 11 ing healed left carpometacarpus after coaptation (Splint and fig- (4.33%), splint and interdigital bandage 3 cases (1.18% each), ure-8 bandage). This bird achieved full flight and was released. and 1 case of ball bandage (0.39%) (Table 3). Fracture Analysis of Wild Birds in South Korea 199

Surgical outcomes istics of fractures in birds, and could also serve as a basic Of the 254 cases, there were 123 (48.42%) mortalities, 81 database for the treatment of fracture in wild birds. This (31.89%) were released, 29 (11.41%) euthanized, 13 (5.12%) study shows a similar pattern of fracture lesions and treat- hospitalized, and 3 (1.81%) found dead on arrival (DOA). ments as has been reported in earlier researches. However, The outcome of the 254 birds is presented in Table 4. there are differences in the survival rate and the prognosis.

Discussion Acknowledgement

According to a previous study, the most common species This work was supported by the Research Resettlement of raptors with fractures was the Common kestrel (Falco tin- Fund for the new faculty of Seoul National University. nunculus), followed by the Northern boobook (Ninox scutulata) (9). However, rescued species in countries such as the References USA, Greece, and Spain were mostly species other than the Common kestrel (Falco tinnunculus) and Northern boobook 1. Arnaud JVW, Larry JW, Craig AB, Joan EB. Mechanical (Ninox scutulata) (10-12,15). The present study also revealed evaluation of external skeletal fixator-intramedullary pin tie-in the unique pattern reported previously for fracture percent- configurations applied to cadaveral humeri from red-tailed hawks Buteo jamaicensis age in Common kestrel (Falco tinnunculus) followed by ( ). J Avian Med Surg 2009; 23: 277-286. Northern boobook (Ninox scutulata). 2. Bennett RA, Kuzma AB. Fracture management in birds. J Zoo Wildl Med 1992; 23: 5-38. The humerus, radius, and ulna were the most frequent sites 3. Bueno I, Redig PT, Rendahl AK. External skeletal fixator of fracture in the present study, which is similar to a previ- intramedullary pin tie-in for the repair of tibiotarsal fractures ous report (9). Furthermore, the percentage of fractures in the in raptors. J Am Vet Med Assoc 2015; 10: 1154-1160. ulna (29.70%) was slightly lower than the previous report 4. Cano FG, Reviriego F, Espinosa AA, Collado CS. Interactive (approximately 50%) (9). avian anatomy: Functional and clinical aspects. Vet Anat 2012. In the present study, we found 2 cases of fractures in the 5. Chinnadurai SK, Strahl-Heldreth D, Fiorello CV, Harms CA. notarium and synsacrum region. The avian vertebral column Best-practice guidelines for field-based surgery and anesthesia exhibits fused, rigid vertebrae such as the notarium, synsa- of free-ranging wildlife. I. Anesthesia and analgesia. J Wildl crum, and pygostyle (2). This rigidity could be the cause of Dis 2016; 52: S14-S27. free thoracic vertebrae being vulnerable to fracture. 6. Hill SC, Lee YJ, Song BM, Kang HM, Lee EK, Hanna A, Moreover, in a previous study, patient reintroduction was Gilbert M, Brown IH, Pybus OG. Wild waterfowl migration and domestic duck density shape the epidemiology of highly reported to be the most frequent outcome of fracture manage- pathogenic H5N8 influenza in the Republic of Korea. Infect ment, followed by captivity; additionally, this study reported Genet Evol 2015; 34: 267-277. a very low death rate (10). Contrarily, the present study reveals 7. Holz P. Coracoid fractures in wild birds: repair and outcomes. a different percentage of outcome, with a higher death rate as Aus Vet J 2003; 81: 469-471. compared to reintroduction of the wild birds into their habi- 8. Kathomdi UY, Parikh PV, Patil DB, Kelawala DN, Tarware tat. In another study, the number of birds not released was VB. Fracture repair in birds-A clinical study. Ind J Vet Surg higher than the released birds (7), which corresponds to the 2016; 37: 51-53. results of the current study. 9. Kim T, Kwon Y. Bone Fractures in Raptors in the Daegu- Activity was minimized by separating the birds and pro- Gyeongbuk Region. J Vet Clin 2016; 33: 261-265. viding them cage rest. Birds were kept in cage rest for 14 to 10. Komnenou AT, Georgopoulou I, Savvas I, Dessiris A. A 21 days after surgery. In the present study, 18.11% birds were retrospective study of presentation, treatment, and outcome of free-ranging raptors in Greece (1997-2000). J Zoo Wildl Med kept for cage rest, which correlates to a previous study report 2005; 36: 222-229. (3). Another study reported application of IM pins in 10 of 11. Molina-López RA, Casal J, Darwich L. Causes of morbidity the 13 surgically treated cases, excluding the 3 cases of ampu- in wild raptor populations admitted at a wildlife rehabilitation tation. Of the 10 cases, ESF was performed in 2 cases and centre in Spain from 1995-2007: a long term retrospective wire fixation in 1 case (9). In the present study, ESF + IM study. PLoS One 2011; 6: e24603. pinning was applied to 53 cases (20.86%), and there were 5 12. Morishita TY, Fullerton AT, Lowenstine LJ, Gardner IA, cases of amputation. Brooks DL. Morbidity and mortality in free-living raptorial The percentage of treatment with ESF + IM pin was higher birds of northern California: a retrospective study, 1983-1994. in a previous study (9) where ESF + IM pin were used in J Avian Med Surg 1998; 12: 78-81. 54% cases, as compared to the present study, wherein ESF + 13. Oryan A, Monazzah S, Bigham-Sadegh A. Bone injury and IM pin and IM pin alone had equal proportions (20.86%). fracture healing biology. Biomed Environ Sci 2015; 28: 57-71. 14. Redig T. A clinical review of orthopedic techniques used in the rehabilitation of raptors. In: Zoo & wild animalmedicine. Conclusion Philadelphia: Saunders 1986: 388-401. 15. Rodríguez B, Rodríguez A, Siverio F, Siverio M. Causes of The current study evaluated fractures in wild birds. The raptor admissions to a wildlife rehabilitation center in Tenerife most common species with fractures was the Common kes- (Canary Islands). J Raptor Res 2010; 44: 30-40. trel (Falco tinnunculus). Ulna was the most frequent site of 16. Westfall ML, Egger EL. The Management of Long Bone fracture. The findings of this study will provide wildlife vet- Fractures in Birds. Iowa State Veterinarian 1979; 2: 81-87. erinarians information regarding the frequency and character-