Origin and Distribution of the Brachial Plexus in the African Giant Pouched Rat (Cricetomys Gambianus- WATERHOUSE, 1840)

Original Article Acta Vet Eurasia 2020; 46: 115-119

Origin and Distribution of the Brachial Plexus in the African Giant Pouched Rat (Cricetomys gambianus- WATERHOUSE, 1840)

Chikera Samuel IBE , Sandra Uchenna BENSON , Ekele IKPEGBU Department of Veterinary Anatomy, Michael Okpara University of Agriculture Umudike, Nigeria Cite this article as: Ibe, C.S., Benson, S.U., Ikpegbu, E., 2020. Origin and Distribution of the Brachial Plexus in the African Giant Pouched Rat (Cricetomys gambianus-WATERHOUSE, 1840). Acta Vet Eurasia 2020; 46: 115-119.

ORCID IDs of the authors: C.S.I. 0000-0001-7612-1982; S.U.B. 0000-0002-9880-4941; E.I. 0000-0003-2553-882X. Abstract

This study examined the origin and distribution of the brachi- trunk, while the caudal trunk was formed by the ventral ramus al plexus in the African giant pouched rat. Ten adult animals of C7, C8, and T1. The peripheral nerve trunks and their respe- (five males and five females) obtained from the wild were ctive spinal nerve origin (in parenthesis) were cranial pectoral used. Cotton blocks were soaked in 2% hydrogen peroxide (C5–C6), suprascapular (C5–C6), cranial subscapular (C5–C7), and placed on the ventral roots of the plexuses to facilitate caudal subscapular (C6–C7), axillary (C6–C7), musculocutane- visualization and tracing. The brachial plexus primarily origi- ous (C7–C8), median (C6–T1), radial (C7–T1), ulna (C7–T1), tho- nated from the caudal branch of the ventral ramus of cervical racodorsal (C6–T1), long thoracic (C7–T1), and lateral thoracic nerve 5 (C5), ventral ramus of cervical nerve 6 (C6), cervical (C8–T1). To summarize, the peripheral nerves of the brachial nerve 7 (C7), cervical nerve 8 (C8), and cranial branch of the plexus displayed some differences when compared with other ventral ramus of first thoracic nerve (T1). The cranial trunk rodents. was formed by the caudal branch of the ventral ramus of C5 and the ventral ramus of C6; two branches originating from Keywords: African giant pouched rat, nerve plexus, peripheral C6 were bound to the cranial part of C7 to form the middle nerves, rodents, spinal nerves

Introduction the spinal cord, is a complex anatomical structure, from its origin in the cervical to its final branching in the axillary region. In Nigeria, some wild rodents such as the African giant It is formed by a set of nerves with origin in the cervical and pouched rat (Cricetomys gambianus) have become an alterna- thoracic segments of the spinal cord and distributed in the tho- tive or a supplementary source of animal protein, and hence, racic girdle, thorax, and forelimb (Souza-Junior et al., 2018). In been raised domestically for their meat. Elsewhere, they serve domestic mammals, the nerve of the brachial plexus is formed as exotic pets (Cooper, 2008). The African giant pouched rat is by a variable pattern of junctions between ventral branches of one of the largest rodents in Africa and is proven to be useful in the fourth, fifth, sixth, seventh, and eighth cervical nerves (C4– disease diagnosis (Maggie, 2003). C8), and the first and second thoracic nerves (T1 and T2) (Mussa The spinal cord is a cylindrical part of the central nervous sys- et al., 2016). Their fibers run across short distances, innervating tem. It exhibits subtle cervicothoracic and lumbosacral en- the skin and muscles of the thoracic limbs. Comparative studies largements in segments that innervate the fore and hindlimbs, of the brachial plexus between species have been developing respectively. An interconnecting network of branching nerve since the 19th century. Understanding the patterns and varia- fibers, known as plexuses, is responsible for the enlargements. tions of the brachial plexus is one of the challenging areas in The brachial plexus, formed at the cervicothoracic junction of gross neuroanatomy.

Address for Correspondence: Chikera Samuel IBE • E-mail: [email protected] This work is licensed under a Creative Received Date: 27.03.2020 • Accepted Date: 27.07.2020 • DOI: 10.5152/actavet.2020.20015 Commons Attribution-NonCommercial Available online at actavet.org 4.0 International License.

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The African giant pouched rat is wild, but aggressively hunted limb using tissue forceps, rat-toothed forceps, Allis forceps, scis- as a bush meat, thus may go extinct. The need to conserve the sors, and scalpel. Bilateral incisions were made near and parallel species calls for an understanding of its biology as a prerequi- to the sternum. The forelimbs were laterally exposed to the ribs. site for its domestication. Works have been conducted on the The ribs were disarticulated, and the sternum was removed for biology of the brachial plexus in other rodents such as the Wis- the evisceration of the thoracic contents; then the muscles tar rat (Uzun et al., 2001), chinchilla (Gamba et al., 2007), red close to the intervertebral foramina were dissected to allow vi- squirrel (Aydin, 2011), naked mole rat (Aydin and Karan, 2012), sualization of the cervical and thoracic nerves. The courses of nutria (Guimaraes et al., 2013), and Spix’s yellow-toothed cavy the nerves emanating from the plexus were exposed. (Araujo et al., 2016). However, the available literature shows that none has been documented for the African giant pouched Tracing the brachial spinal nerves and peripheral nerves of rat. However, the spinal cord anatomy of the rodent has re- the brachial plexus ceived some attention (Olude et al., 2015). Small cotton blocks moistened with 2% hydrogen peroxide were put in position of the brachial plexus to facilitate the vi- The present research will increase available information on the sualization of the nerves and their tracing from their origin. The anatomy of the rodent. Furthermore, it will provide a baseline organization of the main branches of the brachial plexuses of for the future neuroanatomical studies, serve as a guide for local all the African giant pouched rats, irrespective of sex, was in- and regional anesthetic nerve block techniques, and provide vestigated. The peripheral nerves of the brachial plexus were a reference point in further clinical assessments of the spinal identified according to the innervations in muscles of the neck, cord of the African giant pouched rat. Consequently, the aim of arm, forearm, and thorax. Dissections were followed by sketch- this research was to identify the origin of the spinal nerves that es of the different arrangements of the brachial plexus for the form the brachial plexus in the African giant pouched rat, trace analysis and documentation. Nomenclature and definitions of their distribution, and trace the peripheral nerves that emerge gross anatomical structures were based on Nomina Anatomica from the plexus as well as identify the muscles they innervate Veterinaria (2012). The data obtained in the study were pre- in the rodent. sented using photographs and table. Materials and Methods Results and Discussion

Management of the animals Spinal nerves of the brachial plexus The subjects were 10 adult clinically healthy African giant The ventral ramus of C5 was divided into two branches: a cra- pouched rats, consisting of five males and five females. They nial and a caudal branch. The brachial plexus constituted of were captured from the grasslands in and around Mbaise, Imo the caudal branch of the ventral ramus of C5 (Figure 1: red ar- state, Nigeria, using metal cage traps. They were cared for at row), the ventral ramus of C6 (Figure 1: black arrow), C7 (Figure the Histology/Embryology Laboratory of the Department of 1: blue arrow), and C8 (Figure 1: green arrow), and the cranial Veterinary Anatomy, Michael Okpara University of Agriculture branch of the ventral ramus of T1 (Figure 1: orange arrow). This Umudike, Nigeria, in proper hygienic conditions. Before the experiment, they were kept for 1 month to acclimatize to the environment, and were fed with potato tubers, yam tubers, palm kernel fruits, commercial rodent concentrates, and water ad libitum.

The experimental procedure was approved by the Research Ethics Committee, College of Veterinary Medicine, Michael Okpara University of Agriculture Umudike, Nigeria. The ethical approval protocol number assigned to the work is MOUAU/ CVM/REC/2019011. The management of the experimental animals was in accordance with the Guide for the Care and Use of Laboratory Animals, 8th Edition, National Research Council, USA (National Academic Press, Washington D.C.: www.nap.edu.).

Exposure of the vertebral column The rats were sedated with mild inhalation chloroform and weighed using a digital electronic balance (Citizen Scales (1) PVT Ltd., sensitivity: 0.01 kg). They were thereafter euthanized with a higher dose of the gaseous chloroform. Each rat was Figure 1. Ventral view of the brachial plexus of the right placed on lateral recumbency and carefully dissected to re- antimere in African giant pouched rat move the skin, underlying muscles, sternum, and adjacent fore-

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is similar to what has been described for the nutria (Guimar- aes et al., 2013) and Wistar rat (Uzun et al., 2001). Conversely, in the porcupines (Aydin, 2003) and Chinchilla (Gamba et al., 2007), the brachial plexus spanned from C5 to T2. In the gerbil, it originates from C4 to T1 (Araujo et al., 2018). According to Souza-Junior et al. (2018), plexuses that are composed of at least five spinal nerve segments reflect a versatile thoracic limb function that can act, for example, in digging and excavation, climbing fruit trees and houses, running, swimming, and food manipulation. Often, these movements are made naturally by the African giant pouched rat in its habitat.

The caudal branch of ventral ramus of C5 and the ventral ramus of C6 formed the cranial trunk. Two branches originating from the ventral ramus of C6 were bound to the cranial part of the ventral ramus of C7 to form the middle trunk. A caudal part of the ventral ramus of C7 and the ventral ramus of C8 and T1 contributed to the formation of the caudal trunk. Thus, the brachial plexus in the African giant pouched rat, from this study, consisted of cranial, middle, and caudal trunks (Figure 1: black, blue, and orange stars, respectively). This has also been reported in the Wistar rat by Bertelli et al. (1992). In this respect, it Figure 2. Ventral view of the peripheral nerves of the brachial differs from the brachial plexus of the porcupine (Aydin, 2003) plexus of the right antimere in the African giant pouched rat and the white New Zealand rabbit (Mussa et al., 2016), which are formed from cranial and caudal trunks only. It also differs from that of the Chinchilla in which, according to Gamba et al. branch. The axillary nerve originated from C5 and C6 in the red (2007), it is formed by the caudal branch of C5 and the cranial squirrel (Aydin, 2011) and the Mongolian gerbil (Araujo et al., branch of T2 as a single trunk. 2018), unlike the observation in the present study.

Origin of the peripheral nerves of the brachial plexus The musculocutaneous nerve originated from the ventral ra- The peripheral nerves of the brachial plexus from the pres- mus of C7–C8. This is similar to that of the White New Zealand ent study included the cranial pectoral nerve, suprascapular rabbit as reported by Mussa et al. (2016). It differs with that of nerve, cranial subscapular nerve, caudal subscapular nerve, the Wister rat and chinchilla that originates from C5–7 (Berteli axillary nerve, musculocutaneous nerve, median nerve, radial et al., 1992) and from C7 only (Gamba et al., 2007), respectively. nerve, ulnar nerve, thoracodorsal nerve, long thoracic nerve, The median nerve originated from the ventral ramus of C7–T1 and lateral thoracic nerve (Figure 2). They innervated the mus- with a contribution of C6 observed on the left antimere. Araujo cles of the forelimb and lateral thorax. The cranial pectoral et al. (2018) did not report the involvement of C6 in the origin nerve originated from the ventral ramus of C5–C6 (Figure 2). of the median nerve of the Mongolian gerbil. The radial nerve However, Gamba et al. (2007) reported that the origin of this was also formed from the ventral ramus of C7–T1 (Figure 2). The nerve was from C7–T2 in Chinchilla. The suprascapular nerve origin of the radial nerve of the African giant pouched rat from also originated from the ventral ramus of C5–C6 in the animals the present study is similar to that of the nutria as described by studied with a contribution of only C6 observed on the left in Guimaraes et al. (2013). The ulnar nerve arose from the ventral one of the animals. This is similar to the findings of Gamba et ramus of C8 and T1, but, in one case, it had a contribution from al. (2007) in Chinchilla, Aydin (2003) in porcupine, and Mussa C7 on the left antimere nerve. This origin is similar to the porcu- et al. (2016) in White New Zealand rabbits, but differed in Spix’s pine (Aydin, 2003) and the Mongolian gerbil (Araujo et al. 2018) yellow-toothed cavy which was formed by C6 and C7 (Araujo but differs from the report in chinchilla (Gamba et al., 2007) and et al., 2016) and in the Mongolian gerbil (Araujo et al., 2018) white New Zealand rabbit (Mussa et al., 2016) which arose from which was formed by C4 and C5. The cranial subscapular nerve T1 and T2. The thoracodorsal nerve originated from the ventral originated from the ventral ramus of C6–C7; a contribution of ramus of the C6–T1. The long thoracic nerve had its origin in C5 was observed on the left antimere. The caudal subscapular branches from C7–T1. This is similar to the findings in Wistar rat and axillary nerves originated from the ventral ramus of C6– (Uzun et al., 2001), but differ in porcupine (Aydin, 2003) which C7. Reports by Aydin (2003) and Mussa et al. (2016) indicate arose from C7 and C8. The lateral thoracic nerve arose from the that the subscapular nerve in the porcupines and White New ventral ramus of C8–T1 (Figure 2). Conversely, Scavone et al. Zealand rabbits, respectively, was formed by the ventral ramus (2008) reported that the lateral thoracic nerve in the paca was of C5 and C6 and was not divided into a cranial and a caudal formed by roots of C8–T2.

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Table 1. Summary of the origin and muscles innervated by the peripheral nerves of the brachial plexus of the African giant pouched rat S. no Peripheral nerves Origin Muscles 1 Cranial pectoral C5–C6 Superficial pectoralis 2 Suprascapular C5–C6; *C6 Supraspinatus; Infraspinatus 3 Cranial subscapular C6–C7; *C5 Subscapularis 4 Caudal subscapular C6–C7 Subscapularis 5 Axillary C6–C7 Subscapularis; Teres major; Teres minor; Deltoideus 6 Musculocutaneous C7–C8 Coracobrachialis; Brachialis; Biceps brachii 7 Median C7–T1; *C6 Pronator teres; Flexor carpi radialis; Superficial digital flexor; Deep digital flexor; Flexor digiti III, Flexor digiti IV 8 Radial C7–T1 Brachialis; Triceps brachii; Tensor fasciae antebrachii; Extensor carpi radialis; Extensor digitorum lateralis; Ulnaris lateralis; Abductor digiti I longus 9 Ulnar C8–T1; *C7 Cutaneous; Anconeus; Flexor carpi ulnaris; Interossei; Flexor digiti V 10 Thoracodorsal C6–T1 Latissimus dorsi 11 Long thoracic C7–T1 Thoracic belly of serratus ventralis 12 Lateral thoracic C8–T1 Cutaneous trunci *Observed on the left antimere; C: cervical nerve; T: thoracic nerve

The above results showed that the peripheral nerves whose branches to the biceps brachii, brachialis, and coracobrachialis innervations ended on muscles proximal to the cubital joint muscles (Table 1), after arising from the middle trunk. It lay dor- originated from the cranial branches (C5–C7) and were mostly sal to the axillary nerve. Aydin and Karan (2012) described that monosegmental. The other peripheral nerves, which included the musculocutaneous nerve in the mole-rat branched toward radial, median, and ulnar nerves, had their origins concentrat- the cutaneous antebrachii muscle. This was not found in the ed in C7, C8, and T1, respectively. These peripheral nerves were African giant pouched rat in the present study. pluri-segmental. Thus, a largest contingent of nerve fibers to The median nerve arose cranial to the ulnar nerve and in- the complex musculature can be necessary, which move the nervated muscles stated in Table 1. The ulnar nerve provided elbow, carpus, and digits, especially for wild rodents, such as branches to the skin and other muscles including the anconeus the African giant pouched rat, which depends on their limb for (Table 1), unlike in the chinchilla in which Gamba et al. (2007) digging and climbing. reported that the anconeus muscle was not innervated by the Distribution of the peripheral nerves of the brachial plexus ulnar nerve. The radial nerve originated from the cranial part The cranial pectoral nerve arose from the cranial part of the cra- of the caudal trunk, dorsal and caudal to the median nerve. It nial trunk and innervated the superficial pectoral muscle (Fig- provided branches to the three heads of the triceps brachii and ure 2: black star). The suprascapular nerve originated from the other muscles (Table 1). At the elbow joint, it subdivided into caudal part of the cranial trunk, passed between subscapular deep and superficial branches. The deep branch of the radial nerve was found inserted between the brachioradialis and the muscle and supraspinatus muscle, exited at the lateral surface origin of the extensor carpi radialis muscles, innervating the of the scapula, and continued through the supraspinatus and former and distributing to all craniolateral musculature of the infraspinatus muscles, innervating them. The innervation of the Antebrachium. The superficial branch separated into the digi- supraspinatus and infraspinatus muscles by the suprascapular tal dorsal common III and IV nerves at distal antebrachium. The nerve coincides with reports in Spix’s yellow-toothed cavy by thoracodorsal nerve provided branches to the latissimus dorsi Araujo et al. (2016). However, Cruz and Adami (2010) reported muscle. The long thoracic nerve distributed to the thoracic ven- that the suprascapular nerve supplied branches to the deltoid tral serratus muscle. The lateral thoracic nerve branches at the muscle in the wooly monkey. cutaneous muscles of trunk. This innervation has been record- The subscapular was divided into two: the cranial and caudal ed in the paca by Scavone et al. (2008). subscapular nerves. They originated from the point where the Conclusion branch from the cranial trunk joined the middle trunk innervating the subscapular muscle. The axillary nerve originated This study has attempted to demonstrate the morphology of from the middle trunk and after a short distance, splits into the brachial plexus and the distribution of its nerves in the Af- two branches. The muscles they innervate are stated in Table 1. rican giant pouched rat. Nerves originating from the brachial The musculocutaneous nerve (Figure 2: purple arrow) provided plexus displayed some significant differences in African giant

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pouched rat compared with the Wistar rat, paca, chinchilla, Bertelli, J. A., Mira, J.C., Gilbert, A., Michot, G.A., Legagneux, J., white New Zealand rabbits, porcupines, and other rodents. The 1992. Anatomical basis of rat brachial plexus reconstruction. Sur- present findings have added to the literature of rodent brachial gical and Radiologic Anatomy 14, 85-86. [Crossref] plexus. They may also serve as a guide in surgical procedures Cooper, R.G., 2008. Care, husbandry and diseases of the African Giant of the rodent. rat (Cricetomys gambianus). Journal of the South African Veteri- nary Association 79, 62-66. [Crossref] Cruz, G.A.M., Adami, M., 2010. Anatomy of the brachial plexus of the Ethics Committee Approval: Ethics committee approval was received woolly-monkey (Lagothrix lagothricha). Pesquisa Veterinária Bra- for this study from the ethics committee of the College of Veterinary sileira 30, 881-886. [Crossref] Medicine, Michael Okpara University of Agriculture Umudike, Nigeria. Gamba C.O., Castro T.F., Rickes E.M., Pereira M.A.M., 2007. The ner- The ethical approval protocol number assigned to the work is MOUAU/ vous territories of the brachial plexus in Chinchilla lanigera. Bra- CVM/REC/2019011. zilian Journal of Veterinary Research and Animal Science 44, 283- 289. [Crossref] Peer-review: Externally peer-reviewed. Guimaraes, R.T., Birck, A.J., Filadelpho, A.L., Guimaraes, G.C., Bar- Author Contributions: Concept - C.S.I; Design - C.S.I., S.U.B.; Supervi- celos, R.P., 2013. Origem e distribuição do plexo braquial no nu- sion - C.S.I., E.I.; Resources - C.S.I., S.U.B., E.I.; Materials - C.S.I., S.U.B.; Data tria (Myocastor coypus). [Origin and distribution brachial plexus in Collection and/or Processing - C.S.I., S.U.B., E.I.; Analysis and/or Interpre- the nutria (Myocastor coypus)]. The Revista de la Facultad de Me- tation - C.S.I., S.U.B.; Literature Search - C.S.I., S.U.B.; Writing Manuscript dicina Veterinaria y de Zootecnia 20. In Portuguese - C.S.I., S.U.B., E.I.; Critical Review - C.S.I., E.I.; Other - C.S.I., S.U.B., E.I. Maggie, M., 2003. Giant Rats to Sniff out Tuberculosis. Retrieved De- Conflict of Interest: The authors have no conflicts of interest to de- cember 16, 2018 from http://www.NewScientist.com. clare. Mussa, T., Bhowmik, S., Ali, L., Islam, A., Quasem, A., Jalil, A., Shaown, R.H., 2016. Origin and distribution of brachial plexus of Financial Disclosure: The authors declared that this study has received white New Zealand rabbit (Oryctolagus cuniculus). Malaysian Jour- no financial support. nal of Veterinary Research 7, 53-64. References Nomina Anatomica Veterinaria., 2012. International Committee on Veterinary Gross Anatomical Nomenclature, 6th Edition, Hannover Araujo, H.N., Jr., Oliveira, G.B., Costa, H.S., Lopes, P.M.A., Olivei- Columbia. ra, R.E.M., Bezerra, F.V.F., Moura, C.E.B., Oliveira, M.F., 2018. Olude, M.A., Idowu, A.O., Mustapha, O.A., Olopade, J.O., Akinloye, Anatomy of the brachial plexus in the Mongolian gerbil (Meriones A.K., 2015. Spinal cord studies in the African giant rat (Cricetomys unguiculatus Milne-Edwards, 1867). Veterinarni Medicina 63, 476- gambianus, Waterhouse). Nigerian Journal of Physiological Sci- 481. [Crossref] ences 30, 025-032. Araujo, H.N., Jr., Oliveira, G.B., Silva, A.V.N., Oliveira, R.E.M., Ca- mara, F.V., Oliveira, C.M., Jr., Bezerra, F.V.F., Oliveira, M.F., Scavone, A.R.F., Machado, M.R.F., Guimaraes, G.C., Oliveira, F.S., 2016. Origin and distribution of the brachial plexus of the Spix’s Gerbasi, S.H.B., 2008. Origin and distribution analyses of the yellow-toothed cavy (Galea spixii Wagler, 1831) (Rodentia, Cavii- brachial plexus perifheral nerves of paca (Agouti paca Linnaeus, dae). Veterinarni Medicina 61, 337-343. [Crossref] 1766). Ciência Animal Brasileira 9, 1046-1055. Aydin, A., 2003. Brachial plexus of the porcupine (Hystrix cristata). Vet- Souza-Junior, P., Carvalho, N.C., Dowich, G., Nogueira, D.M.P., erinarni Medicina 48, 301-304. [Crossref] Anjos, B.L., Santos-Sousa, C.A., Abidu-Figueiredo, M., 2018. Aydin, A., 2011. The spinal nerves that constitute the brachial plexus in Origin and antimeric distribution of brachial plexus nerves in the red squirrel (Sciurus vulgaris). Veterinarni Medicina 56, 405-408. Alouatta guariba clamitans Cabrera, 1940 (Primates: Atelidae), The [Crossref] European Zoological Journal 85, 362-371. [Crossref] Aydın, A., Karan, M., 2012. The spinal nerves forming the brachial Uzun, A., Cengiz, N., Kavakli, A., Karakas, S., 2001. Morphological plexus in mole-rats (Spalax leucodon). Veterinarni Medicina 57, and microscopical examination of the rat brachial plexus. Turkish 430-433. [Crossref] Journal of Veterinary and Animal Sciences 25, 397-402.

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