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Origin and insertion of the nerves constituting the braquial plexus of the roadside hawk

Abstract

The roadside hawk (Rupornis magnirostris) is a free-living bird that commonly has wing injuries caused by man-made obstacles when flying. Studies that describe the topographic anatomy of the wings of this species are necessary to assist in the treatment of possible wing lesions. For this reason, the present work aimed to describe the origin and insertion of the nerves that constitute the brachial plexus in roadside hawks. Five roadside hawk carcasses donated to the Animal Anatomy Laboratory of the São Judas University Center, UNIMONTE campus, by CEPTAS (Center for Research and Screening of Wild Animals) were used for the study. The brachial plexus of the roadside hawk was formed by the union of the ventral branches of the spinal nerves located between C9-C10-T1-T2-T3. The ventral branches joined together and formed four short trunks which later united again by exchanging nerve fibers and constituting a big caliber branch. This is divided into two nerve cords (dorsal and ventral) which are destined to specific muscular groupings. The dorsal cord originates the axillary, anconeal and radial nerves, and is responsible for innervating the extensor muscles. The ventral cord originates the pectoral, bicipital, median-ulnar, median and ulnar nerves, and is responsible for innervating the flexor muscles.

Key words
Rupornis magnirostris; wing; Brachial Plexus; anatomy; birds

INTRODUCTION

The great diversity of Brazilian territory (flora and fauna) allows the existence of a large number of taxonomic groups (ICMBIO 2018ICMBIO. 2018. http://www.icmbio.gov.br/portal/faunabrasileira.
http://www.icmbio.gov.br/portal/faunabra...
). The roadside hawk (Rupornis magnirostris), also known by the names of anajé, indaié-hawk, inajé, ripino, indaié and pega-pinto, is a bird of the accipitridae family observed from Mexico to Argentina. It is classified as a bird of prey, meaning a carnivorous bird that presents certain adaptations for active hunting (Santos & Rosado 2009SANTOS WM & ROSADO FR. 2009. Dados Preliminares da Biologia do Gavião-Carijó (Rupornismagnirostris, Gmelin, 1788) na Região Nordeste do Pará. Revista em Agronegócios e Meio Ambiente 2: 421-430., Santos et al. 2009SANTOS WWMS, COPATTI JF & ROSADO FR. 2009. Nidificação de gavião-carijó Rupornis magnirostris (Falconiformes, Accipitridae) no município de Peabiru (Paraná, Brasil). SaBios: Revista de Saúde e Biologia 4: 52-55.). It is not currently considered endangered according to the International Union for Conservation of Nature (IUCN 2018IUCN. 2018. IUCN Red List of Threatened Species. Versão 2017.3. Disponível em: <www.iucnredlist.org>. Acesso em: 10 jun. 2018.
www.iucnredlist.org...
), being the most abundant and well-distributed hawk in Brazil (Sick 1997SICK H. 1997. Ornitologia brasileira. Rio de Janeiro: Editora Nova Fronteira, 912 p.).

The roadside hawk is characterized by a sharp and curved beak, well-developed and strong claws, as well as excellent vision and hearing, giving this animal hunting ability (Brown 1997BROWN L. 1997. Birds of prey (2nd ed.). London: Chancellor Press, 256 p., Silva 2016SILVA RMN. 2016. Descrição anatômica do plexo braquial em corujas das espécies Athene cunicularia e Tyto furcata. Final term paper. Universidade de Brasília, Brasília, Brasil.). It presents a great variation in its plumage colors according to the region of the country. However, it stands out for its finely bared chest of the belly and the tail with several clear stripes in contrast to the dark gray bands or black. Males and females are practically the same except in relation to size, with the female being larger. It feeds on large insects, lizards, small snakes, birds such as ground doves and sparrows, and can also catch bats in daytime landings (Robinson 1994ROBINSON SK. 1994. Habitat selection and foraging ecology of raptors in Amazonian Peru. Biotropica 26: 443-458., Sick 1997SICK H. 1997. Ornitologia brasileira. Rio de Janeiro: Editora Nova Fronteira, 912 p.).

Exacerbated anthropic activity promotes changes in the biome, promoting the destruction of several habitats (Ramos et al. 2011RAMOS CCO, BENEDITO E & ZAWADZKI CH. 2011. Dieta e conteúdo calórico de aves atropeladas na região central do estado do Paraná, Brasil. Biotemas 24: 153-170.). Free-living birds such as the roadside hawk are often susceptible to injury due to accidents with human-imposed obstacles (ICMBio 2018ICMBIO. 2018. http://www.icmbio.gov.br/portal/faunabrasileira.
http://www.icmbio.gov.br/portal/faunabra...
, Ministério do Meio Ambiente 2003MINISTÉRIO DO MEIO AMBIENTE. 2003. Secretaria de Biodiversidade e Florestas. Fragmentação de ecossistemas: causas, efeitos sobre a biodiversidade e recomendações de políticas públicas, 99 p. Disponível em: <http://www.mma.gov.br/estruturas/chm/_arquivos/fragment.pdf>. Acesso: 10 jun. 2018.
http://www.mma.gov.br/estruturas/chm/_ar...
). Thus, complex structures of the wings like the nerves that constitute the brachial plexus become compromised, preventing their flight and consequently excluding them from their habitat.

Wing muscles are innervated by nerves coming from the brachial plexus. The nerve roots (origin of the nerves) pass through the lateral cervical musculature and are suddenly found to form the trunks of the brachial plexus. Most branches from the trunks are ventrally viewed from the scapula and caudally to the humerus (Baumel 1986BAUMEL JJ. 1986. Sistema nervoso das aves. In: Getty R (5th ed.), Sisson/Grossman: Anatomia dos Animais Domésticos. Rio de Janeiro: Guanabara Koogan, p. 1890-1929., Brenner et al. 2010BRENNER DJ, LARSEN RS, DICKINSON PJ, WACK RF, WILLIAMS DC & PASCOE PJ. 2010. Development of an Avian Brachial Plexus Nerve Block Technique for Perioperative Analgesia in Mallard Ducks (Anas platyrhynchos). J Avian Med Surg 24: 24-34., Dyce et al. 2010DYCE KM, SACK WO & WENSING CJG. 2010. Tratado de Anatomia Veterinária (4th ed.). Rio de Janeiro: Elsevier, 856 p.). The study of the brachial plexus is extremely important for early diagnosis of diseases that affect the brachial plexus (Shell et al. 1993SHELL L, RICHARDS M & SAUNDERS G. 1993. Brachial plexus injury in two red-tailed hawks (Buteo jamaicensis). J Wildl Dis 29: 177-179.), as well as for adequate therapeutic management for both surgical repair of wing fractures (Gizah et al. 2008GIZAH GC, SANTOS MGA, CORAIOLA AM, SILVA LCS, LANGE RR & SANTIN E. 2008. Doenças de aves selvagens diagnosticadas na Universidade Federal do Paraná (2003-2007) Pesq Vet Bras 28: 565-570.) and for the anesthetic protocols in this region (Soresini et al. 2013SORESINI GG, PIMPÃO CT & VILANI RGD’OC. 2013. Bloqueio do plexo braquial em aves. Rev Acad Agrar Ambient 11: 17-26.). For this reason, the present work has the aim of describing the origin and insertion of the nerves that constitute the brachial plexus in roadside hawks (Rupornis magnirostris).

MATERIALS AND METHODS

Five female roadside hawk carcasses (Rupornis magnirostris) were used to the study. They were donated frozen to the Animal Anatomy Laboratory of the São Judas University Center, UNIMONTE campus, by CEPTAS (Center for Research and Screening of Wild Animals).

The roadside hawks were fixed with 10% formaldehyde solution and then packaged in the same solution for a minimum period of 48 hours. Dissection was performed by incision, folding the skin and subcutaneous tissue of the axillary region, followed by removing the sternum, along with the pectoral and supracoracoid muscles through the section of the ribs, coracoid bone and clavicle, exposing and individualizing the nerves composing the brachial plexus in both antimeres.

The nerve roots were individualized near the vertebral column in order to observe which ventral branches of the cervical and thoracic spinal nerves contribute to forming the brachial plexus. Thus, the cervical vertebrae and the first pair of ribs were identified. After identification of these levels, nerve dissection was then performed. The brachial plexus arrangement was documented and the nomenclature used for the anatomical description is according to the Avian Anatomical Nomenclature (Baumel 1993BAUMEL JJ. 1993. Handbook of avian anatomy: nomina anatomica avium (2nd ed.). Cambridge, Nuttall Ornithological Club.).

RESULTS

The brachial plexus of the roadside hawk (Rupornis magnirostris) is formed by the union of the spinal nerve ventral branches located between the ninth cervical vertebra and the third thoracic vertebra (C9-C10-T1-T2-T3). The ventral branches from origin (roots) form the short nerve trunks (four short trunks) that join, promoting an exchange of fibers and forming a big caliber trunk outside the coelomic cavity (Figure 1a) which divides into nerve cords extended to specific muscle groups (Figure 1b-c).

Figure 1
Photomacrographs of the brachial plexus of the roadside hawk (Rupornis magnirostris). a-b: ventral view; c: medial view; d: side view. Scale bar: 1.0cm. Legend: C9- Ninth cervical vertebra, C10- tenth cervical vertebra, T1- first thoracic vertebra, T2- second thoracic vertebra, T3- third thoracic vertebra, 1- origin of first short nerve trunk, 2- origin of the second short nerve trunk, 3- origin of the third short nerve trunk, 4- origin of the fourth short nerve trunk, A- short trunk; B- ventral branch, Bm- median-ulnal nerve, Bp- bicipital nerve, C- dorsal branch, Ca- axillar nerve, Can- anconal nerve, Cr - radial nerve.

The first nerve stem originated from the intervertebral space between C9 and C10. This short nervous trunk emitted an isolated nervous filament, which did not join with the other short trunks, following directly to the rhomboid, sternocoracoid and supracoracoid muscles (Figure 1a). The first (between C9-C10) and the fourth (T2-T3) short nerve trunks presented a more tenuous appearance when compared to the second (between C10-T1) and the third (T1-T2) short trunks, which were thicker (Figure 1a).

The four short trunks formed together into a single, fairly thick trunk, dividing into two nervous cords after passing through the wall of the coelomic cavity. However, a nervous filament originating from the fourth short trunk does not join, advancing directly to the arm and inserting into the humerus triceps and scapulo-triceps muscles.

The ventral and dorsal cords followed directly to the arm. The pectoral nerve arose from the initial portion of the ventral cord at its cranial border, which followed horizontally and emitted its nerve branches to the pectoral muscle. Afterwards, the bicipital nerve was verified in the more cranial portion of the arm, innervating the biceps brachial muscle. The ventral cord then continued to the medial region of the arm as a median-ulnar nerve, which continued its course to the cubital fossa where it divided into median nerve and ulnar nerve. The median-ulnar nerve is exposed in the medial region of the arm. The branches of the ventral cord supply the ventral (flexor) compartment muscles of the limb (Figure 1b-c).

The axillary nerve emerged in the initial portion of the dorsal cord, which went to the dorsal portion of the shoulder. Afterwards, the dorsal cord continued to the arm as a radial nerve. The anconeal nerve appeared from the caudal surface of the radial nerve, very close to the origin of the axillary nerve, innervating the humerus triceps muscle (Figure 1b-c). The radial nerve contoured the humerus to the lateral region of the arm in its proximal third, being visualized superficially in the middle and distal third of the humerus without any muscular protection (Figure 1d). The branches of the dorsal cord supply the dorsal (extensor) compartment muscles of the limb and the overlying skin.

DISCUSSION

The study of the brachial plexus in birds, especially in wild birds, is not only important for morphological knowledge, but also for the early diagnosis of diseases that affect the plexus and compromise their flight. These disorders can include acute injuries as a result of trauma, usually the main cause of the radial nerve paralysis (midair collisions, automobile accidents, gunshots, bite wounds, lacerations and iatrogenic damage during surgical procedures and injection of therapeutic agents) (Antolitou et al. 2012ANTOLITOU A, KAZAKOS G & PRASINOS NN. 2012. Peripheral nerve damage in companion animals Hellenic. J Companion Animal Med 12: 12-19., Shell et al. 1993SHELL L, RICHARDS M & SAUNDERS G. 1993. Brachial plexus injury in two red-tailed hawks (Buteo jamaicensis). J Wildl Dis 29: 177-179.). Moreover, even the radial nerve rupture is possible, due to its proximity to the diaphysis of the bone and the small amount of musculature present in the region (Bolson et al. 2005BOLSON J, MACHADO G, ZEMBRZUSKI F & SCHOSSLER JE. 2005. Fratura umeral exposta e ruptura do nervo radial em coruja de orelha (Rhipnoptyns clamator). In: ENCONTRO DE ZOOLÓGICOS DO RIO GRANDE DO SUL, I, Cachoeira do Sul. Anais... Cachoeira do Sul: ONG Acaang. Versão eletrônica.). Besides, an avulsion or tearing of these nerves root can also occur (Stephen & Smith 1993STEPHEN A & SMITH DVM. 1993. Diagnosis of brachial plexus avulsion in three free-living owls. In: Redig PT. Raptor biomedicine. University of Minnesota Press: Minneapolis, p. 99-102.). In this case, the damage can be permanent, including lack of pain perception, muscle atrophy and paralysis with loss of reflexes (Ritchie et al. 1994RITCHIE BW, HARRISON GJ & HARRISON JR. 1994. Avian Medicine: principles and application. Florida: Wingers Publishing, 397 p.).

Furthermore, the morphological knowledge is essential for surgical approach, such as fractures corrections (Bolson & Schossler 2008BOLSON J & SCHOSSLER JEW. 2008. Osteossíntese em aves: revisão bibliográfica. Arquivo de Ciências Veterinárias e Zoologia da Unipar 11: 55-62.) or amputation (which is required when infections, neoplasias, severe radial nerve paralysis or chronic malunion fractures compromise the systemic health of the patient) (Latney et al. 2018LATNEY L, RUNGE J, WYRE N, LARENZA-MENZIES MP, NEVILLE C & BRISCOE J. 2018. Novel Technique for Scapulohumeral Amputations in Avian Species: A Case Series. Israel J Vet Med 73: 35-45.). In addition, this knowledge is extremely useful for local and regional anesthetic procedures (Vilani et al. 2006VILANI RGOC, FERREIRA FM, LANGE RR & SAMONEK JFV. 2006. Brachial plexus block in birds. Exotic 8: 27-32., Soresini et al. 2013SORESINI GG, PIMPÃO CT & VILANI RGD’OC. 2013. Bloqueio do plexo braquial em aves. Rev Acad Agrar Ambient 11: 17-26., Balthazar 2016BALTHAZAR DA. 2016. Desenvolvimento de técnica para bloqueio dos nervos medianoulnar e radial em patos (Cairina moschata). [43 f.]. Tese de doutorado (PROGRAMA DE PÓS-GRADUAÇÃO EM MEDICINA VETERINÁRIA (PATOLOGIA E CIÊNCIAS CLÍNICAS) - Universidade Federal Rural do Rio de Janeiro, [Seropédica-RJ]., Nascimento et al. 2019NASCIMENTO FM, NUNES TL, SOUZA TBS, ANDRADE MAC & BARBOSA VF. 2019. Bloqueio do plexo braquial com uso de neuroestimulador em coruja-orelhuda (clamador da Ásia) submetido à amputação de asa. Acta Sci Vet 47: 361., Credie et al. 2019CREDIE LFGA, MENDES JCFS, CORREA AM & FUTEMA F. 2019. Bloqueio do plexo braquial em gavião-asa-de-telha (Parabuteo unicinctus) com auxílio do estimulador de nervos periféricos: relato de caso. Singular 1: 11-14.). The lack of information regarding the distribution and location of the brachial plexus nerves in these animals may be a limiting factor for such procedures.

The spinal nerves that constitute the brachial plexus of birds may vary among species since there are variations between the number of vertebrae in each region (Nickel et al. 1977NICKEL R, SCHUMMER A & SEIFERLE E. 1977. Anatomy of the domestic birds. Berlin: Parey, 202 p.). Information about the origin and insertion of the nerves that constitute the brachial plexus of the roadside hawk (Rupornis magnirostris) is scarce, so the present research conducted a comparison with other bird species.

Roadside hawks presented four nerve origins (or roots) located between the vertebrae C9-C10, C10-T1, T1-T2 and T2-T3. Although the nervous origin varies among birds due to the different number of vertebrae in each region, hens presented similarity to the roadside hawks, having the origin of their plexus between the last two cervical segments and the first three thoracic segments (Nickel et al. 1977NICKEL R, SCHUMMER A & SEIFERLE E. 1977. Anatomy of the domestic birds. Berlin: Parey, 202 p.). In the present study, it was observed that in the vulture (Coragyps atratus foetens) (Moreira et al. 2009MOREIRA PRR, SOUZA NTM & CARVALHO RG. 2009. Arranjos configurados pelos nervos do plexo braquial no urubu (Coragyps atratus foetens). Braz J Vet Res Anim Sci 46: 144-151.), the burrowing owl (Athene cunicularia), the american barn owl (Tyto furcata) (Silva 2016SILVA RMN. 2016. Descrição anatômica do plexo braquial em corujas das espécies Athene cunicularia e Tyto furcata. Final term paper. Universidade de Brasília, Brasília, Brasil.) and blue fronted amazon parrots (Amazona aestiva) (Silva et al. 2015SILVA RMN, FIGUEIREDO PO & SANTANA MI. 2015. Formação e distribuição do plexo braquial em papagaios verdadeiros (Amazona aestiva, Linnaeus, 1758). Ci Anim Bras 16: 464-473.) also presented four nervous origins at the cervicothoracic junction, but between different vertebral levels. Differently, Franceschi et al. (2009)FRANCESCHI RC, SOUZA DAS, PROVENCI M & PEREIRA MAM. 2009. Estudo da inervação e vascularização do membro torácico de Columba livia. Braz J Vet Res Anim Sci 46: 507-514. reported only three nervous origins in pigeons (Columba livia), as well as Nickel et al. (1977)NICKEL R, SCHUMMER A & SEIFERLE E. 1977. Anatomy of the domestic birds. Berlin: Parey, 202 p. in ducks (Anas platyrhynchos) and geese (Anser anser), Moreira et al. (2005)MOREIRA PRR, SOUZA WM, SOUZA NTM, CARVALHO RG & CUSTÓDIO AA. 2005. Arranjos configurados pelos nervos do plexo braquial no peru (Meleagris gallopavo). ArsVeterinaria 21: 296-302. in turkeys (Meleagris gallopavo), and Achôa Filho et al. (2014)ACHÔA FILHO K, RODRIGUES MN, FONSECA ET, LEANDRO RM, PASQUALETTI VB & MIGLINO MA. 2014. Origem, distribuição e inserção dos nervos do plexo braquial em araras canindé (Ara ararauna, Linnaeus, 1758). Biotemas 3: 157-166. in the blue-and-yellow macaw (Ara ararauna).

As previously verified, there is no standardization defined in the brachial plexus of birds (Nickel et al. 1977NICKEL R, SCHUMMER A & SEIFERLE E. 1977. Anatomy of the domestic birds. Berlin: Parey, 202 p.). This variability in the number of origins is probably related to the size and quantity of cervical and thoracic vertebrae, a fact that can modify the number of intervertebral foramina, directly influencing the point of origin of the nerve trunks.

The short nerve trunks are formed after the exit of the nerves through the intervertebral foramina, in which there is an interchange of fibers (Baumel 1986BAUMEL JJ. 1986. Sistema nervoso das aves. In: Getty R (5th ed.), Sisson/Grossman: Anatomia dos Animais Domésticos. Rio de Janeiro: Guanabara Koogan, p. 1890-1929.). These trunks cross a triangular hiatus when emerging from the coelomic cavity, cranially occupying this space (Soresini et al. 2013SORESINI GG, PIMPÃO CT & VILANI RGD’OC. 2013. Bloqueio do plexo braquial em aves. Rev Acad Agrar Ambient 11: 17-26.). The roadside hawks presented four nervous origins that constituted four short trunks, similar to the blue fronted amazon parrots (Silva et al. 2015SILVA RMN, FIGUEIREDO PO & SANTANA MI. 2015. Formação e distribuição do plexo braquial em papagaios verdadeiros (Amazona aestiva, Linnaeus, 1758). Ci Anim Bras 16: 464-473.) and the burrowing owl (Silva 2016SILVA RMN. 2016. Descrição anatômica do plexo braquial em corujas das espécies Athene cunicularia e Tyto furcata. Final term paper. Universidade de Brasília, Brasília, Brasil.). The vulture also presents four nervous origins, but with the formation of three short trunks (Moreira et al. 2009MOREIRA PRR, SOUZA NTM & CARVALHO RG. 2009. Arranjos configurados pelos nervos do plexo braquial no urubu (Coragyps atratus foetens). Braz J Vet Res Anim Sci 46: 144-151.). Turkeys (Moreira et al. 2005MOREIRA PRR, SOUZA WM, SOUZA NTM, CARVALHO RG & CUSTÓDIO AA. 2005. Arranjos configurados pelos nervos do plexo braquial no peru (Meleagris gallopavo). ArsVeterinaria 21: 296-302.) and blue-and-yellow macaws (Achôa Filho et al. 2014ACHÔA FILHO K, RODRIGUES MN, FONSECA ET, LEANDRO RM, PASQUALETTI VB & MIGLINO MA. 2014. Origem, distribuição e inserção dos nervos do plexo braquial em araras canindé (Ara ararauna, Linnaeus, 1758). Biotemas 3: 157-166.) present three origins with the formation of three short trunks. In the American barn owl, Silva (2016)SILVA RMN. 2016. Descrição anatômica do plexo braquial em corujas das espécies Athene cunicularia e Tyto furcata. Final term paper. Universidade de Brasília, Brasília, Brasil. reported the presence of five short trunks.

In the same way that it was observed in the dissected roadside hawks, the specific literature consulted was unanimous in reporting the union of the brachial plexus forming nerve trunks in a common trunk, with dorsal and ventral cords separating and whose branches respectively supply the nerves of the extensor compartments, the wing flexor, and overlying skin. The nerves coming from the dorsal cord observed in the hawks were the axillary nerve, the anconeal nerve and the radial nerve. These nerves are responsible for innervating the wing extensor musculature and are also found in the turkey (Moreira et al. 2005MOREIRA PRR, SOUZA WM, SOUZA NTM, CARVALHO RG & CUSTÓDIO AA. 2005. Arranjos configurados pelos nervos do plexo braquial no peru (Meleagris gallopavo). ArsVeterinaria 21: 296-302.), in the burrowing and American barn owls (Silva 2016SILVA RMN. 2016. Descrição anatômica do plexo braquial em corujas das espécies Athene cunicularia e Tyto furcata. Final term paper. Universidade de Brasília, Brasília, Brasil.), in the vulture (Moreira et al. 2009MOREIRA PRR, SOUZA NTM & CARVALHO RG. 2009. Arranjos configurados pelos nervos do plexo braquial no urubu (Coragyps atratus foetens). Braz J Vet Res Anim Sci 46: 144-151.), and in the blue fronted amazon parrot (Silva et al. 2015SILVA RMN, FIGUEIREDO PO & SANTANA MI. 2015. Formação e distribuição do plexo braquial em papagaios verdadeiros (Amazona aestiva, Linnaeus, 1758). Ci Anim Bras 16: 464-473.). There is no description of the anconal nerve in the pigeon (Franceschi et al. 2009FRANCESCHI RC, SOUZA DAS, PROVENCI M & PEREIRA MAM. 2009. Estudo da inervação e vascularização do membro torácico de Columba livia. Braz J Vet Res Anim Sci 46: 507-514.). The nerves that emerge from the ventral cord are the pectoral nerve, bicipital nerve, median-ulnar nerve, median nerve and ulnar nerve, which innervate the wing flexor muscles, and are the same described in the mentioned species.

CONCLUSION

An important detail observed regarding the distribution of the brachial plexus nerves was the location of the radial and median-ulnar nerves; the radial nerve is superficially found at the humerus without muscular protection when transpassing from the medial to lateral aspect, which suggests fragility in the peripheral system, as well as the median-ulnar nerve in the medial view, with these areas being susceptible to traumas.

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Publication Dates

  • Publication in this collection
    29 Oct 2021
  • Date of issue
    2021

History

  • Received
    10 Oct 2019
  • Accepted
    15 June 2020
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