Bilateral multiple complex variations in the formation ... - Springer Link

Surg Radiol Anat (2009) 31:723–731 DOI 10.1007/s00276-009-0503-1

A N A T O M I C V A R I A T IO N S

Bilateral multiple complex variations in the formation and branching pattern of brachial plexus Anjali Aggarwal · K. Harjeet · Daisy Sahni · Aditya Aggarwal

Received: 8 January 2009 / Accepted: 30 March 2009 / Published online: 22 April 2009 © Springer-Verlag 2009

Abstract Bilateral variations in the formation and branching of brachial plexus are extremely rare. Multiple bilateral variations in brachial plexus right from divisions to branching pattern were observed during the dissection in an adult male cadaver. Lateral and medial cord formation showed deviation from the usual pattern. Anterior division of upper trunk continued as lateral cord. Medial cord was formed by the union of anterior division of lower trunk and anterior division of middle trunk, thus receiving Wbers from both the trunks. Anterior division of middle trunk bifurcated into upper and lower branches. We encountered two lateral roots bilaterally and two medial roots of median nerve on the left side with anomalous origin. There were three upper subscapular nerves on the left and two on the right side with variations in their origin. Anomalous origin of many other branches on both sides was encountered. It is extremely uncommon to Wnd so many variations in one body and bilateral variations are still too rare. Understanding of such variations is clinically important for diagnosing unexplained clinical signs and symptoms as well as during nerve blocks and certain surgical procedures around the neck and proximal arm. Keywords Bilateral

Brachial plexus · Anatomy · Variation ·

Anjali Aggarwal · K. Harjeet · D. Sahni Department of Anatomy, Postgraduate Institute of Medical Education and Research, Chandigarh, India Anjali Aggarwal (&) 123-C Old Type V Sector 24-A, Chandigarh, India e-mail: [email protected] Aditya Aggarwal Department of Orthopaedic Surgery, Postgraduate Institute of Medical Education and Research, Chandigarh, India e-mail: [email protected]

Introduction Brachial plexus is simply visualized as beginning with ventral rami of spinal nerves C5, C6, C7, C8 and T1 in the neck and terminating as Wve terminal branches musculocutaneous, median, ulnar, radial and axillary nerves in axilla. The intermediate portion is displayed as three trunks, divisions and cords [12, 18]. However, brachial plexus may sometime show deviation from this common pattern in any of its part. Important variations exist in the brachial plexus [8, 9]. The deWnitive peripheral nerves leaving the plexus are composed of Wbers from several segments. Thus, their branches to the individual muscle may contain Wbers from at least two segments [7]. The branches of brachial plexus may vary considerably in their levels of origin, probably much less frequent with regard to Wbers they contain. They do vary in the later respect also, and these variations may be clinically more important since they account for the variations in segmental innervation of muscles. At times the anatomy of brachial plexus is quite confusing because of frequent variations. Many variations have been reported in past by various authors. Their usefulness becomes still more signiWcant for anesthetists, surgeons and even radiologists as these variations are the constant challenge during surgical interventions. Data on this subject comes from anatomical studies usually encountered during routine cadaver dissections [4, 7]. This study presents bilateral, multiple and complex anatomical variations in the formation and branching pattern of brachial plexus observed during routine educational dissection.

Materials and methods A case of bilateral multiple complexities in the brachial plexus was found in a 50-year-old embalmed male cadaver,

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during routine educational dissection at the department of anatomy, Postgraduate Institute of Medical Education and Research, Chandigarh, during academic year 2007–2008. For better visualization of continuity of nerves in the cervical region, middle two-thirds of clavicle was sectioned on both sides. An attempt was made to trace the origin of each nerve proximally in neck up to the roots macroscopically. Findings were immediately photographed and lengths of necessary nerves were measured with a sliding vernier caliper (accuracy 0.02 mm; Mitutoyao, Kawasaki, Kanagawa, Japan). The anatomical diagrams were drawn to demonstrate the radicular origin of each nerve for simplicity and better understanding.

Results Left side Unusual variations were observed in the course of brachial plexus (Table 1). Variation in the formation of lateral cord was noticed as it was formed solely by anterior division of upper trunk without receiving any contribution from anterior division of middle trunk. After descending for 9 mm, it gave oV its Wrst branch, lateral pectoral nerve in the supraclavicular region; after coursing for further 45 mm, it terminated into musculocutaneous nerve and lateral root of the median nerve (Figs. 1, 2). Lateral pectoral nerve received an additional contribution from the upper branch of anterior division of Middle trunk. Thus, its formation by fusion of two roots was an anomalous Wnding. Anterior division of middle trunk divided into upper and lower branches which was a rare variation. Upper branch further subdivided into three smaller branches: one each communicating with the lateral pectoral nerve, lateral root of median nerve (LRMN) and medial root of the median nerve (C1. C2. C3 in Figs. 1, 2). Lower branch after giving few Wbers to the medial pectoral nerve joined the anterior division of lower trunk to form the medial cord (Figs. 1, 2). Thus, variation was observed in medial cord formation with additional C7 Wbers from the anterior division of middle trunk. The medial cord as usual terminated into ulnar nerve and medial root of median nerve (MRMN). However, Wber content of these terminal branches was anomalous, as they contained extra C7 Wbers besides C8 and T1. Medial cord before termination gave a branch, which bifurcated into medial cutaneous nerve of arm and medial cutaneous nerve of forearm. An additional branch arose from the anterior division of lower trunk, which further divided into medial cutaneous nerve of arm and medial cutaneous nerve of forearm (Figs. 1, 2). Thus, variation in number and source of origin of both medial cutaneous nerve of

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arm and medial cutaneous nerve of forearm was found. Medial pectoral nerve originating from anterior division of lower trunk was joined by another above-mentioned root from lower branch of anterior division of middle trunk in a variant manner. Unusual origin of suprascapular and two upper subscapular nerves (US1 and US2 in Fig. 3) from posterior division of upper trunk, 19, 21, 24 mm, respectively, distal to point of its origin was observed. Posterior division of all three trunks joined in a usual manner to form posterior cord (Fig. 3). Posterior cord received maximum contribution from upper trunk followed by middle and lower trunks. Length of posterior division of upper, middle and lower trunks was 41, 28, 25 mm, respectively, whereas thickness was 3.6, 2.1 and 0.6 mm, respectively. Posterior cord divided into two terminal branches: axillary and radial nerves. Lower subscapular and thoracodorsal nerve arose from axillary and radial nerves, respectively in a variant manner (Fig. 3). Formation of median nerve In our study, rare variation of presence of two lateral and two medial roots of median nerve was noticed. The thicker main lateral root arising from lateral cord was joined by an additional thinner lateral root (C2 in Figs. 1, 2) arising from the upper branch of anterior division of middle trunk, just distal to its origin, to form LRMN proper. Similarly, the thicker main medial root arising from medial cord was joined by an additional thinner medial root (C3 in Figs. 1, 2) arising from upper branch of anterior division of middle trunk, to form MRMN proper. The axillary artery was found to be traversing between the two medial roots of median nerve (Figs. 1, 2) before formation of MRMN proper. Finally, median nerve was formed by the union of LRMN proper and MRMN proper (Figs. 1, 2). Right side On the right side, lateral cord formation was unusual as it was a continuation solely of the anterior division of the upper trunk (length of lateral cord: 71 mm). Thus, like left side it contained Wbers of only C5 and C6 (Figs. 7, 8). After giving unusually high origin to lateral pectoral nerve in the supraclavicular region, lateral cord terminated as musculocutaneous nerve and lateral root of the median nerve. Anterior division of middle trunk gave a branch, which after traversing for a short distance divided into two sub branches: (1) second lateral pectoral nerve and (2) another, united with a branch from anterior division of lower trunk to form a loop which splitted into two medial pectoral nerves (Figs. 4, 5). Like left side, both lateral and medial pectoral nerves originating from two diVerent sources were anomalous in formation, origin and


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Table 1 Variations in formation and branching of brachial plexus Present study

Standard described anatomy

Lateral cord

AD of UT

BL

C5, 6

AD of UT & AD of MT

Musculocutaneous

AD of UT

BL

C5, 6

Lateral cord

C5, 6, 7

Lateral root of median nerve

AD of UT

BL

C5, 6

Lateral Cord

C5, 6, 7

Suprascapular

PD of UT

BL

C5, 6

Upper subscapulara

PD of UT BL

US1 US2

C5, 6, 7

UT

C5, 6

PC (single)

C5, 6

PC

C5, 6

C5,6 (R) C5 (L)

BL

C6 (BL)

R

C6, 7

US3

PC

Lower subscapular

Axillary

L

C5, 6

PC

R

C6, 7

Radial nerve

L

C6, 7, 8

PC

C6, 7, 8

1. UB

BL

C7

Does not occur

–

Does not occur

–

Does not occur

–

AD of LT

C8, T1

MC (single)

C8T1

MC (single)

C8 T1

C7, 8, T1

MC

C8 T1

C5, 6

LC (single)

C5,6,7

MC (single)

C8, T1

Lateral cord

C5, 6, 7

Medial cord

C8, T1

Thoracodorsal Anterior division of middle trunk

2. LB UB of AD of MT

C7

1. LPN

R

2. LR of MN

C7

3. MR of MN UB of AD of MT

C7

1. CBM (b1,b3)

L

2. LR of MN Medial cord

C7

C7 C7

LB of AD of MT & AD of LT

BL

C7 C8, T1

Medial cutaneous nerve of arm (n = 2)

1. AD of LT

L

2. MC Medial cutaneous nerve of forearm (n = 2)

1. AD of LT

C8 L

2. MC MC

BL

Lateral root of median nerve (n = 2)

1. AD of UT

BL

2. UB of AD of MT 1. UB of AD of MT

C7 L

2. MC Lateral pectoral nerve (n = 2)b

1. AD of UT 1. AD of MT

C7 C8, T1

BL

2. AD of MT Medial pectoral nerve (n = 2)c

T1 C8

Ulnar nerve

Medial root of median nerve (n = 2)

T1

C5, 6, 7 (R) C6, 7 (L)

BL

C7, 8

2. AD of LT BL bilateral, R right, L left, CBM coracobrachialis muscle, UB upper branch, LB lower branch, for rest of abbreviations see Fig. 1 a Upper subscapular (n = 2 on left side; n = 3 on right side) b Lateral pectoral nerve (n = 2) join together to form one on left; remain separate on right c Medial pectoral nerve (n = 2) join together to form one on left; join to form a loop before separating again on right

numbers. Anterior division of the middle trunk divided into upper and lower branches (Figs. 4, 5) which were unusual as seen on the left side, but further branching was diVerent and variant. Upper branch descended medial to the axillary artery and terminated by dividing into three branches; two branches (b1 and b3) entered the medial surface of the coracobrachialis muscle while the third branch (b2; accessory lateral root of the median nerve) joined the thicker main lateral root of the median nerve (a branch of lateral cord) to form lateral root of the median

nerve proper (Figs. 4, 5). Anterior division of lower trunk, after giving medial pectoral nerve and a common branch which bifurcated into medial cutaneous nerve of arm and medial cutaneous nerve of forearm, joined lower branch of anterior divisions of the middle trunk to form the medial cord, which terminated by dividing into the medial root of the median nerve and the ulnar nerve (Figs. 4, 5). The course, branching pattern of anterior division of the middle trunk and medial cord formation were anomalous. Posterior division of upper trunk gave unusual origin to

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Fig. 1 Left brachial plexus. UT upper trunk, MT middle trunk, LT lower trunk, ADU anterior division of upper trunk, PDU posterior division of upper trunk, SN suprascapular nerve, US1 Wrst upper subscapular nerve, LPN lateral pectoral nerve, MPN medial pectoral nerve, UBAD upper branch of anterior division of middle trunk, LBAD lower branch of anterior division of middle trunk, LC lateral cord, PC posterior cord, MC medial cord, AA axillary artery, UN ulnar nerve, MCN


musculocutaneous nerve, LRMN lateral root of median nerve, MRMN medial root of median nerve, MCNA medial cutaneous nerve of arm, MCNFA medial cutaneous of forearm, C1 communicating branch between UBAD of MT and LPN, C2 communicating branch between UBAD of MT and LRMN, C3 communicating branch between UBAD of middle trunk and MRMN, Inf inferior, sup superior, med medial, lat lateral

Fig. 2 Schematic diagram of left brachial plexus. For abbreviations see Fig. 1

Fig. 3 Left brachial plexus showing the formation of trunks, divisions and branching pattern of posterior cord (after retracting medial and lateral cords). UT upper trunk, PDU posterior division of upper trunk, ADU anterior division of upper trunk, PDM posterior division of

middle trunk, PDL posterior division of lower trunk, PC posterior cord, SN suprascapular nerve, US1 Wrst upper subscapular nerve, US2 second upper subscapular nerve, AX axillary nerve, LS lower subscapular nerve, RN radial nerve, TD thoracodorsal nerve

suprascapular, Wrst and second upper subscapular nerves (US1 and US2) about 20, 22 and 29 mm, respectively, distal to its point of formation. Length of posterior division

of upper, middle and lower trunks was 32, 18 and 22 mm, respectively, whereas the thickness was 3.2, 2.0 and 0.6 mm, respectively. The length of posterior cord was

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Fig. 4 Right brachial plexus. b1 & b3 branches from UB of AD of MT to coracobrachialis muscle, b2 communicating branch from UB of AD of MT to LRMN. For rest of the abbreviations see Fig. 1

Fig. 5 Schematic diagram of right brachial plexus. For abbreviations see Figs. 1and 4

30 mm. After giving third upper subscapular (US3), thoracodorsal and lower subscapular nerves, it terminated as radial and axillary nerves (Fig. 6). Thus, there were three upper subscapular nerves on the right side that was anomalous in number and origin. Formation of median nerve On the right side, there were two lateral roots of median nerve and only one medial roots of the median nerve. The thicker main lateral root arising from lateral cord was

joined by an additional thinner lateral root (b2 in Figs. 4, 5) arising from upper branch of anterior division of middle trunk to form LRMN proper. Two lateral roots of the median nerve were unusual in number and origin. Median nerve was formed by the union of LRMN proper and MRMN. Apparent radicular origin of various nerves as observed macroscopically after dissection proximally into the neck is depicted in Figs. 7 and 8 and Table 1. However, the possibility of microscopic interconnections between the nerves can not be ruled out.

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Fig. 6 Right brachial plexus showing formation of trunks, divisions and branching pattern of posterior cord (after retracting lateral cord and medial cord). US1 Wrst upper subscapular nerve, US2 second upper subscapular nerve, US3 third upper subscapular nerve. For rest of abbreviations see Figs. 1and 3

Fig. 7 Apparent radicular origin of peripheral branches of left brachial plexus. For abbreviations see Figs. 1and 3

Discussion The segregation of developing structures within the limb bud has a directive action upon the growing nerve Wbers and subsequently grouping into deWnite bundles. The presence of anomalies may be attributed to random factors inXuencing the mechanism of formation of limb muscles and the peripheral nerves during embryonic life [13]. The knowledge of variations of peripheral nervous system is useful in clinical as well surgical practice as they may be the cause of nerve palsy syndromes because of variable relations of nerves and related muscles. Owing to more reliance on computer imaging in diagnostic medicine, variations of brachial plexus are vulnerable to injury during the routine surgical procedures in neck. In the present study, bilateral multiple variations were observed in the formation and branching pattern of brachial plexus.

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Many studies have reported the variations of the entire brachial plexus [8, 11]. There is paucity of literature available speciWcally studying variation of lateral cord in detail. In a series reported by Kerr [8], lateral cord apparently contained Wbers either from the C4, C5, C6 and C7 nerves or C5, C6 and C7 in all the cases. No case with lateral cord having only C5 and C6 Wbers was found. Uzun and Bilgic [16] reported formation of lateral cord from anterior division of the upper trunk only in four out of 130 cases (3.07%) on right side. In the present study, on both sides, the lateral cord was derived purely from the anterior division of the upper trunk without any contribution from the middle trunk. Hence, its terminal branches seemed to contain Wbers of only C5 and C6. C7 Wbers instead of joining lateral cord entered medial cord. Thus, lateral cord along with its terminal branches was deWcient of C7 Wbers where as medial cord contained extra C7. Few Wbers from anterior


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Fig. 8 Apparent radicular origin of peripheral branches of right brachial plexus. For abbreviations see Figs. 1, 3, and 6

division of middle trunk joined LRMN thus supplying C7 Wbers to it thus making up the deWciency. In this respect, musculocutaneous nerve deserves special mention as it supplies muscles of the anterior compartment of arm; all muscles of this compartment lacked C7 Wbers. In the study by Kerr [8], musculocutaneous nerve contained C7 Wbers in almost 95% cases. In the present study, coracobrachialis muscle on the right side received C7 Wbers by branches (b1and b3 in Figs. 7, 8) from anterior division of middle trunk which entered the muscle independently. Besides bilateral incomplete lateral cord, another important notable feature on both sides was higher level of formation of lateral cord in the posterior triangle of the neck instead of that in the axilla. Thus, it may be vulnerable to injury during any operative procedure in neck. Gacek [5] in his study observed that an unusual brachial plexus anatomical variant rendered it vulnerable to injury in radical or modiWed neck dissection. Such variations should be known before any brachial plexus block procedure or for vascular or nervous surgery in the neck or in the axillary region. Suprascapular nerve in our study originated from posterior division of upper trunk instead of usual origin from upper trunk on both the sides. Similar variable origin of this nerve from the posterior division of upper trunk on both sides was reported by Fazan et al. [4] and Kerr [8]. Thus, origin of suprascapular nerve was little distal to its common site of origin, i.e., upper trunk. Distal shift of origin probably results in diminution of length of suprascapular nerve. Hence, it could be associated with increased vulnerability.

This fact needs to be kept in mind during mobilization of nerve in entrapment neuropathy [3]. In the present study, lateral pectoral nerve originated by two roots from anterior division of the upper trunk and middle trunk separately on both sides. On the left side, these two roots united by the connective tissue, whereas on the right side two roots remained separate. On the right side, root derived from upper trunk contained only C5 and C6 Wbers on left side C6 Wbers only. The deWciency of C7 Wbers was compensated by additional root from middle trunk. Besides highly unusual pattern of lateral pectoral nerve formation, the level of origin was also higher in our study. Owing to its origin from divisions of trunk, it may be injured during surgery in posterior triangle of neck. Kerr [8] in his extensive work on brachial plexus, found a single root of origin in about 24%, two roots in about 55% and three roots in about 20%, but these were not always from separate sources, i.e., both roots either arising from the lateral cord or one from anterior division of the upper trunk and other from lateral cord. He also mentioned Wber composition varying from C4 through C7. Like lateral pectoral nerve, medial pectoral nerve too demonstrated dual roots from anterior division of middle trunk and lower trunk on both sides. In Kerr’s study [8], medial pectoral nerve was found to be the Wrst branch of medial cord in 69.59% and in next 24.5% cases it arose from the lower trunk or the anterior division of lower trunk and in the remainder, from C8 or MRMN. Although in majority of cases, it receives Wbers from C8 and T1, but may receive from C7 also [8] as seen

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in our case. Loukas et al. [10], in some of their cases observed similar variations in number and source of pectoral nerves and laid emphasis on clinical importance of these variations in surgeries such as limb neurotization, mastectomy, and orthopedic procedures. In the present study anterior division of the middle trunk instead of joining anterior division of the upper trunk, bifurcated into upper and lower branches on both right and left sides. The further fate of these branches was still more complicated; upper branch on left gave rise to one of the two roots of lateral pectoral nerves, few Wbers joined the LRMN and the remaining Wbers descended lateral to axillary artery and joined the MRMN. Lower branch of anterior division of the middle trunk joined with anterior division of lower trunk and few Wbers separated as medial pectoral nerve. Such a pattern of bifurcation of anterior division of middle trunk and then somewhat complicated branching was unique in our study. To our knowledge, this pattern of branching and distribution of anterior division of middle trunk has not been reported in the literature. The Medial cord formation showed deviation from standard described anatomy on both sides as it also contained Wbers from anterior division of middle trunk (C7) in addition to C8 and T1 Wbers from lower trunk. Medial cord is commonly formed by anterior division of lower trunk (C8, T1) only. Kerr [8] in his series of 175 cases found C7 Wbers along with C8 and T1 in medial cord in only six cases. Median nerve is most frequently formed by union of two roots: single lateral root from lateral cord and single medial root from the medial cord. Goyal et al. [6] reported two lateral roots of median nerve arising from the lateral cords bilaterally and single medial root. In our study, median nerve was formed by fusion of four roots on the left side and three roots on the right side. On the left side, one each originated from the lateral and medial cords respectively and remaining two from the anterior division of middle trunk, whereas on the right side three roots were found arising from lateral cord, anterior division of middle trunk and medial cord respectively. Uzun and Seelig [17] in their study reported formation of median nerve by fusion of four roots on the left side: three originating from the lateral cord and one from the medial cord. MRMN doubled on the left with additional root (C3 in Fig. 1) arising from anterior division of middle trunk. Both roots of median nerve closely hugged the axillary artery from medial and lateral sides which may result in compression of axillary artery [1]. In the present study, doubling of medial cutaneous nerve of arm and forearm was seen on the left side. Both nerves arose from common trunks, which in turn originated from the medial cord and anterior division of lower trunk, respectively. On the right side, anomalous source of medial cutaneous nerve of arm and forearm in the form

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a common trunk from anterior division of lower trunk instead of medial cord, was seen in our study. To our knowledge, such Wnding bilaterally with doubling has not been reported in the literature. Fazan et al. [4] in his study reported origin of medial cutaneous nerve of arm and forearm from common trunk only on right side arising from inferior trunk in two cases. However, there was no mention of doubling of these nerves. Medial cutaneous nerve of arm and forearm commonly receive Wbers from both C8 and T1 [18]. In our study on the left side, one of medial cutaneous nerve of arm and forearm received Wbers from C8 and other, from T1, whereas on the right side both nerves derived Wbers from C8 and T1. According to Hollinshead [7], both nerves commonly contain Wbers derived from T1 only. Multiple upper subscapular nerves were observed bilaterally from posterior division of upper trunk and posterior cord: three on the right and two on the left. Few studies have reported such variations in the literature [4, 8, 15]. According to Bergman et al. [2] this nerve may arise from C4, C5 or C6 spinal nerves. In our study, similar origin was observed in Wrst and second subscapular nerves. However, third nerve on the right side contained Wbers derived from C6 and C7. Lower subscapular nerve in addition to usual C5 and C6 Wbers also contained those from C6 and C7 on the right side. Anomalous origin of thoracodorsal and lower subscapular nerve on the left side from radial nerve and axillary nerve, respectively in the present study, was also reported by Fazan et al. [4] and Kerr [8]. According to Tountas and Bergman [14], divisions of trunks and formation of cords may be anomalous, however, arrangement of terminal branches remain unchanged. Thus brachial plexus is merely a routing mechanism to get nerves with common function into the proper terminal nerves. Hence, errors in distribution may occur that are corrected distally in the arm, forearm or hand resulting in anatomical variations of the brachial plexus [14].

Conclusion Brachial plexus may sometime show deviation from its common pattern in any of its part thus leading to anomalous formation. The unique feature in our study was presence of plethora of anomalies in a single cadaver on both sides involving diVerent levels of formation and branching of brachial plexus, not previously reported in literature. Knowledge of such anomaly is clinically important so as to avoid injury to various nerves during surgical procedures in the neck or in axilla. Acknowledgment The authors wish to thank Mr. Vijay Bakshi senior artist of department of anatomy for drawing illustrations.


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