Macroanatomical Investigation of the Plexus Brachialis in the Red Fox (Vulpes vulpes)

The red fox (Vulpes vulpes) is widely distributed all over the world, including Siberia, India, Europe, Asia, North Africa, America, the North Pole, and throughout Turkey (Demirsoy, 2003). These animals generally live in forests, fields and mountains and their survival is largely based on their ability to feed on a great variety of food items such as wild and domestic birds, mice, moles, all insects and their larva, slugs, worms, lizards, and fish. In addition, they sometimes eat fruit. This type of diet contributes to the environmental balance (Bakaloudis et al., 2015; Sidorovich et al., 2006).

The red fox is labeled as a carnivore and has characteristic properties such as a slender pointed muzzle, prominent erect ears, long slender legs, and relatively small feet. The front legs have a very important role in land digging and food grabbing (Demirsoy, 2005). The brachial plexus innervates to the front legs and the plexus brachialis and branches radiate within the front legs. They generally originate from ventral branches of the C6, C7, C8, T1 and T2 spinal nerves (Evans and de Lahunta, 2013; König and Liebich, 2015). Anatomically, the origin, course, or distribution of the plexus brachialis has been studied in many domestic and wild animals such as the cat (Mencalha et al., 2014), New Zealand rabbit (Mohiuddin et al., 2011), chinchilla (Cevik-Demirkan et al., 2007), rat (Ozbag et al., 2009), red squirrel (Aydin, 2011), marten (Demiraslan et al., 2015), bonobo (Kikuchi et al., 2011), pampas fox (Souza et al., 2016), and crab-eating fox (Souza et al., 2014b). Nevertheless, the anatomy of the plexus brachialis of the red fox, which is a wild carnivore, is still unknown and there is a paucity of literature available on the subject. We aimed to describe the origin and branches of the plexus brachialis of the red fox.

This study was performed with permission from the General Directorate of Nature Conservation and National Parks of the Ministry of Forestry and Water region (Permission Number: 38002405-445.05-177733). This study was also accepted by the animal experiments local ethics committee (2017/6-14) of Cukurova University.

This study was performed by using six male red foxes that were collected at different time intervals as a result of road traffic accidents in the Adana region. The animals were all older than six months, as assessed by their dental maturity. Body weight varied from 6 to 9 kg. The animals were stored in a freezer, then fixed in a 10% formalin solution at room temperature for dissection. To demonstrate the plexus brachialis, the soft tissue, muscle, fascia and fat were removed and carefully dissected. For terminology, the Nomina Anatomica Veterinaria (Anonymous, 2017) was used.

The plexus brachialis and its branches are known to vary among species and even within the same species. The plexus brachialis and its branches in the six red foxes examined summarized in Table I. In four of the six animals, the right plexus brachialis consisted of ventral branches from the C6, C7, C8 and T1 spinal nerves, while in the remaining two foxes it originated from C5, C6, C7, C8, T1 and T2. The left plexus brachialis originated from C6, C7, C8 and T1 ventral branches of spinal nerves in all six animals. We observed the plexus brachialis to vary in shape in different areas. These nerves generally passed disto-caudally and in the lateral aspect of the arteria axillaris was observed. The right plexus brachialis was stronger and more defined than the left plexus brachialis and the branches of the right side showed complete and significant connections with each other. In each plexus an ansa axillaris structure was not formed in all six animals.

The nervus (N.) suprascapularis (b in Fig. 2) originated from the left ventral branches of C6, C7 in four animals and the C8 spinal nerve in two animals. The right side (b in Fig. 1) originated from the ventral branches of C5, C6 and C7 in four red foxes and only C7 in two animals. The left nervi (Nn.) subscapulares (a in Fig 2) comprised ventral branches from C6 and C7 spinal nerves in all animals. However, the right nerves (a in Fig. 1) were formed by ventral branches of C5, C6, and C7 spinal nerves in two animals. The left N. musculocutaneus (c in Fig. 2) originated from ventral branches of C8 and T1 spinal nerves in all six foxes while the right (c in Fig. 1) side originated from only C7 in all animals.

The left N. axillaris (d in Fig. 2) originated from the ventral branches of C7 and C8, and the right (d in Fig. 1) side originated from the ventral branches of C7. When N. axillaris separated from the plexus brachialis, both a ventral and caudal course was observed.

While the left nn. pectorales craniales originated from C7, C8 and T1 in two animals, it’s the origin was C8 (e in Fig. 2) in four animals. The right nn. pectorales craniales (e in Fig. 1) was derived from C6 and C7 in four animals, and C7 and C8 in two animals. The nerve branched into three and five in two animals, whereas it diverged into 2 or 4 branches in four animals.

The left N. thoracicus longus (l in Fig. 2) originated from the ventral branches of C7 and C8 in four animals and only C8 in two animals. The right nerve (l in Fig. 1) was formed from the ventral branches of C7 and C8 in all six foxes.

The left N. thoracodorsalis (j in Fig. 2) was formed from ventral branches of C8 and T1 in all cases. The right side of this nerve (j in Fig. 1) was derived from C8 and T1 in three animals, and T1 and T2 in the other three.

The Nn. pectorales caudales (k in Figs. 1, 2) and N. thoracicus lateralis (right and left) (i in Fig. 1) both originated from the ventral branches of C7 and C8 in all six foxes.

N. radialis (f in Fig. 2) was derived from the ventral branches of C6-C7 in the left side, and ventral branches of C6-C7 in four animals and C8 in two animals in the right side (f in Fig. 1). N. radialis was very thick.

Right and left N. medianus (g in Figs. 1, 2) was formed by ventral branches from C8 and T1 in all cases. A connecting branch between N. medianus and N. musculocutaneus was observed in all animals. In three animals, N. medianus and N. ulnaris showed a common trunk.

Both right and left N. ulnaris (h in Figs. 1, 2) originated from ventral branches of C7, C8 and T1 in all six foxes. We also observed that N. medianus and N. ulnaris ran a parallel course, except in one animal.

The plexus brachialis and its branches are well known to show variations among species and even within the same species. Formation of the plexus comprises C5-T1 in myocastor coypus (Pop and Penteathe, 2007), the giant anteater (Souza et al., 2014a), and bonobo (Kikuchi et al., 2011), C5-T2 in cats (Mencalha et al., 2014), and the chinchilla (Cevik-Demirkan et al., 2007), C6-T1 in sheep and goats (Sisson et al., 1975), pampas fox (Souza et al., 2016) and crab-eating fox (Souza et al., 2014b), and C6-T2 in Anatolian sheep dogs (Kangal dog) (Dursun et al., 1994), horses, cattle and pigs (König and Liebich, 2015; Sisson et al., 1975). In addition, the plexus has been reported to occur as two roots in the hippopotamus (Yoshitomi et al., 2012), and as three roots from the ventral branch of C5-8 in the red squirrel (Aydin, 2011). While Angelica-Almeida et al. (2013) reported that the plexus originates between C4 and T1 in rats, Ozbag et al. (2009) suggested that it is between C5 and T1 in the same animals. On the other hand, a mole-rat (Aydin and Karan, 2012) plexus brachialis study showed similar results to those of Ozbag et al. (2009). In the present study on the red fox, we showed that the plexus brachialis originated from C5, C6, C7, C8, T1 and T2, similar to that seen in cats (Mencalha et al., 2014) and the chinchilla (Cevik-Demirkan et al., 2007). Our results indicate similarities with cats rather than dogs.

N. suprascapularis originates from ventral branches of either C6 alone or C6-7 in the crab-eating fox (Souza et al., 2014b), C6-7 in the Anatolian sheep dog (Kangal dog) (Dursun et al., 1994), C4-6, C5-6 or only C6 in Macaca mulatta (Santos-Sousa et al., 2016), and C6 alone, or C6-7 or C7-8 in the pampas fox (Souza et al., 2016). In the present study, the right N. suprascapularis was formed from ventral branches belonging to C5-7 or C7 alone. The left N. suprascapularis originated from ventral branches from C6-7 or only C8.

Nn. subscapulares is separated from the dorsal section of the plexus in the bonobo (Kikuchi et al., 2011), and the cranial trunk in hippopotamus (Yoshitomi et al., 2012), and originates from C6-7 in the Anatolian sheep dog (Kangal dog) (Dursun et al., 1994). Moreover, these nerves are divided into two branches in the cat (Mencalha et al., 2014), bonobo (Kikuchi et al., 2011), and hippopotamus (Yoshitomi et al., 2012). These nerves originate from C6-C7 or only C6 ventral braches, and are separated as four branches in Macaca mulatta (Santos-Sousa et al., 2016). In the giant anteater (Souza et al., 2014a) nn. subscapularis is derived from C5-7, and from C6-7 in the pampas fox (Souza et al., 2016). In the present study, the left nn. subscapulares originated from the ventral branch of C6-7, consistent with that reported for the Anatolian sheep dog (Kangal dog) (Dursun et al., 1994) and pampas fox (Souza et al., 2016).

N. musculocutaneus is observed to originate from C7-C8 in most animals, however, in the pampas fox (Souza et al., 2016) it is reported to derive from nerve branches between C6-T1. It is generally derived from C6-7 in the crab-eating fox (Souza et al., 2014b). N. musculocutaneus is formed from the C7 spinal nerve alone in the marten (Demiraslan et al., 2015) and Anatolian sheep dog (Kangal dog) (Dursun et al., 1994). It originates from the C5-C7 spinal nerves on both the right and left sides of Macaca mulatta (Santos-Sousa et al., 2016), however, in the majority of these animals it is C6-C7. In the chinchilla (Cevik-Demirkan et al., 2007), this nerve derives only from the C7 spinal nerve. In the present study N. musculocutaneus originated only from C7 on the right side and C8-T1 on the left side.

N. axillaris is derived from only C7, C6-8 or C7-8 ventral branches in the pampas fox (Souza et al., 2016), from C7 alone, C6-7, C6-8 or C7-8 in the crab-eating fox (Souza et al., 2014b), and C7 alone in the marten (Demiraslan et al., 2015). Both the right and left N. axillaris is formed from C6-C7 spinal nerves in Macaca mulatta (Santos-Sousa et al., 2016) and chinchilla (Cevik-Demirkan et al., 2007). In the present study, the left N. axillaris was formed from C7-8 spinal nerves similar to the Anatolian sheep dog (Kangal dog) (Dursun et al., 1994).

Nn. pectorales craniales in the pampas fox (Souza et al., 2016) and the crab-eating fox (Souza et al., 2014b) is derived from the ventral branches of C6-7, C7 alone, C7-T1, C8 alone or C8-T1, and from C7 alone in the marten (Demiraslan et al., 2015) and Anatolian sheep dog (Kangal dog) (Dursun et al., 1994). Both sides of nn. pectorales craniales originate from C6 alone, C6-7, C7-8-T1 or C8-T2 in Macaca mulatta (Santos-Sousa et al., 2016). In the chinchilla (Cevik-Demirkan et al., 2007) these nerves comprise ventral branches from C7-8 or T1-2 spinal nerves. In the present study we observed that the left nn. pectorales craniales originated from C7-T1 or C8 while the right side was derived from either C6-7 or C7-8 spinal nerves.

N. thoracicus longus is generally derived from the C7 spinal nerve in animals (Dursun et al., 1994; Souza et al., 2014b, 2016). In the marten (Demiraslan et al., 2015) it derives from the ventral branches of C7-8, and in the chinchilla (Cevik-Demirkan et al., 2007), (one side) and both sides of Macaca mulatta (Santos-Sousa et al., 2016) it originates from C6-7, C7 alone, or C6-8. In the present study, we observed that the left N. thoracicus longus was formed from either C7-8 or C8 alone. The right side of this nerve was as reported in the literature (Demiraslan et al., 2015).

N. thoracodorsalis originates from C7-8, C8 alone, C7-T1 or C8-T1 in the pampas fox (Souza et al., 2016), and C8 alone, C6-7, C7-8, C8-T1 or C7-T1 in the crab-eating fox (Souza et al., 2014b). In both the marten (Demiraslan et al., 2015) and Anatolian sheep dog (Kangal dog) (Dursun et al., 1994) the right side originates from C7-8 while in Macaca mulatta (Santos-Sousa et al., 2016) the right side is derived from C7-8 or C8-T2 and from C7-8, C8-T1 or C8-T2 on the left side. In the chinchilla (Cevik-Demirkan et al., 2007), it derives only from C8. In the present study on the red fox, the left side of N. thoracodorsalis originated solely from C8-T1, while the right side was from either C8-T1 or T1-T2.

N. thoracicus lateralis and nn. pectorales caudalis originate from C8 alone, T1 alone, C7-T1, or C8-T1 in the pampas fox (Souza et al., 2016), from C7-8 in the marten (Demiraslan et al., 2015), T1-2 in the chinchilla (Cevik-Demirkan et al., 2007), C8-T2 in the Anatolian sheep dog (Kangal dog) (Dursun et al., 1994), and C8 alone, T1 alone, C7-T1, C8-T1, C6-7 or C7-8 in the crab-eating fox (Souza et al., 2014b). In the present study, these nerves were formed from the C7-8 spinal nerves, similar to that reported for the marten (Demiraslan et al., 2015).

N. radialis derives from C7-8, C7-T1 or C8-T1 in the pampas fox (Souza et al., 2016) and C7-8, C7-T1, C8-T1 or C6-8 in the crab-eating fox (Souza et al., 2014b). In the marten (Demiraslan et al., 2015) it originates from C8-T1, and C7-T1 in the Anatolian sheep dog (Kangal dog) (Dursun et al., 1994). In Macaca mulatta (Santos-Sousa et al., 2016) the right side N. radialis is formed from C7-8, and C8-T2 in the chinchilla (Cevik-Demirkan et al., 2007). In the present study, while the left side N. radialis was formed from C6-7, the right side originated from C6-8. Contrary to the literature (Dursun et al., 1994), N. radialis was observed to be a fairly thick compared to other nerves in the red fox.

N. ulnaris is reported to have the same origins as N. medianus in the pampas fox (Souza et al., 2016), crab-eating fox (Souza et al., 2014b), and the marten (Demiraslan et al., 2015). It originates from C8-T2 in the Anatolian sheep dog (Kangal dog) (Dursun et al., 1994) and in Macaca mulatta (Santos-Sousa et al., 2016), as well as C8-T1 in Macaca mulatta (Santos-Sousa et al., 2016), and is derived from T1-2 in the chinchilla (Cevik-Demirkan et al., 2007). In the present study, it originated from C7-T1, unlike any previous reports (Demiraslan et al., 2015; Dursun et al., 1994; Souza et al., 2014b, 2016). In addition, we observed that N. ulnaris and N. medianus ran parallel (except for one animal).

N. medianus is derived from C7-8, C7-T1, C8-T1 or T1 alone in the pampas fox (Souza et al., 2016), from C7-T1, C8-T1 or T1 alone in the crab-eating fox (Souza et al., 2014b), from C8-T1 in the marten (Demiraslan et al., 2015), C7-T2 in the Anatolian sheep dog (Kangal dog) (Dursun et al., 1994), C6-T1 or C6-T2 in Macaca mulatta (Santos-Sousa et al., 2016), and C7-T1 in the chinchilla (Cevik-Demirkan et al., 2007). We observed that N. medianus was derived from C8-T1 in the red fox. In addition, we noted that N. medianus and N. ulnaris were seen in a common root in three red foxes.

We conducted a macroanatomical investigation of the plexus brachialis and its branches in the red fox. We observed that the right plexus brachialis was generally formed from C5, C6, C7, C8, T1 and T2 of the rami ventralis of the spinal nerves. The left plexus brachialis comprised C6, C7, C8 and T1. The right plexus brachialis had a regular appearance. We showed that there were differences between the right and left sides in the red fox and that the branches and origin of the plexus brachialis were very similar to cats and the marten. This information may be very beneficial to veterinarians, surgeons and biologists working with wild animals or in zoos.

The authors declare no conflict of interest.