13
ORIGINAL COMMUNICATION Classifying Musculocutaneous Nerve Variations ROBERTO A. GUERRI-GUTTENBERG * AND MARIANA INGOLOTTI Department of Anatomy, School of Biomedical Sciences, Austral University, Pilar, Buenos Aires, Argentina A total of 56 upper limbs from fetuses and adult cadavers were dissected to re- cord anatomical variations in the musculocutaneous nerve (MC). A systematic literature review was performed to identify current classifications of MC varia- tions. Communications were seen between the MC and median nerves in 53.6% of the dissections from which 84.6% were proximal, 7.7% distal, and 7.7% had one proximal and one distal communication to the point of entry of the MC into coracobrachialis muscle. In six out of 54 dissections where the MC was present, the nerve did not pierce the coracobrachialis muscle. In two cases, the MC was absent and in one case the MC and the median nerve had a distal origin. This article describes current classifications of MC variations and their problems. A new classification is proposed combining preexisting ones into an integrated and more detailed overview. Clinical manifestations of iso- lated MC injury with and without the presence of anatomical variations are thoroughly discussed. The knowledge of these variations will allow physicians to correctly interpret anomalous innervation patters of the upper limb. Clin. Anat. 22:671–683, 2009. V V C 2009 Wiley-Liss, Inc. Key words: musculocutaneous nerve; anatomical variations; classification; isolated musculocutaneous nerve injury; absence of musculocu- taneous nerve; communicating branches INTRODUCTION The brachial plexus innervates muscles, joints, and skin of the upper limb by means of supraclavic- ular and infraclavicular branches. The latter come from the lateral, medial, and posterior cords of the brachial plexus. The lateral cord gives rise to the lat- eral root of the median nerve, the lateral pectoral nerve, and the musculocutaneous nerve. The axons forming the 2 mm in diameter musculocutaneous nerve can be traced back to the spinal nerves C5, C6, and C7 (Buch-Hansen, 1955; Standring, 2004). The course of the musculocutaneous nerve (MC) is traditionally described as follows: After a 6.7 6 1.6 cm distance from its origin (Macchi et al., 2007), it pierces the coracobrachialis muscle and descends laterally in between the biceps brachii and brachialis muscle. It supplies the coracobrachialis before the nerve enters the muscle. Branches to the biceps bra- chii and brachialis are supplied after the MC has pierced the muscle, approximately 14.1 6 1 cm from its origin (Macchi et al., 2007). In the elbow, it perfo- rates the deep fascia lateral to the tendon of biceps and continuous as the lateral cutaneous nerve of the forearm (Testut and Latarjet, 1954; Standring, 2004). The relationship in between the MC and the cora- cobrachialis muscle was first observed by the Italian anatomist Giulio Casserio (1556–1616), pupil of Fab- ricius and teacher of William Harvey (1578–1657) at Padua (Diab, 1999; Lee, 2000). Subsequently, the nerve has also been known as nervus perforans Cas- serii or perforating nerve of Casserius (Testut and Latarjet, 1954; Diab, 1999). Variations in the musculocutaneous nerve have been discussed and classified by various authors (Le Minor, 1990; Kosugi et al., 1992; Yang et al., 1995; Venieratos and Anagnostopoulou, 1998; Choi et al., *Correspondence to: Roberto Andre ´s Guerri-Guttenberg, Depart- ment of Anatomy, Facultad de Ciencias Biome ´dicas, Hospital Uni- versitario Austral Juan Domingo Pero ´n 1500, Pilar, Buenos Aires B1664INZ, Argentina. E-mail: [email protected] Received 15 January 2009; Revised 26 March 2009; Accepted 3 June 2009 Published online 27 July 2009 in Wiley InterScience (www. interscience.wiley.com). DOI 10.1002/ca.20828 V V C 2009 Wiley-Liss, Inc. Clinical Anatomy 22:671–683 (2009)

Classifying musculocutaneous nerve variations

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ORIGINAL COMMUNICATION

Classifying Musculocutaneous Nerve Variations

ROBERTO A. GUERRI-GUTTENBERG* AND MARIANA INGOLOTTI

Department of Anatomy, School of Biomedical Sciences, Austral University, Pilar, Buenos Aires, Argentina

A total of 56 upper limbs from fetuses and adult cadavers were dissected to re-cord anatomical variations in the musculocutaneous nerve (MC). A systematicliterature review was performed to identify current classifications of MC varia-tions. Communications were seen between the MC and median nerves in53.6% of the dissections from which 84.6% were proximal, 7.7% distal, and7.7% had one proximal and one distal communication to the point of entry ofthe MC into coracobrachialis muscle. In six out of 54 dissections where the MCwas present, the nerve did not pierce the coracobrachialis muscle. In twocases, the MC was absent and in one case the MC and the median nerve had adistal origin. This article describes current classifications of MC variations andtheir problems. A new classification is proposed combining preexisting onesinto an integrated and more detailed overview. Clinical manifestations of iso-lated MC injury with and without the presence of anatomical variations arethoroughly discussed. The knowledge of these variations will allow physiciansto correctly interpret anomalous innervation patters of the upper limb. Clin.Anat. 22:671–683, 2009. VVC 2009 Wiley-Liss, Inc.

Key words: musculocutaneous nerve; anatomical variations; classification;isolated musculocutaneous nerve injury; absence of musculocu-taneous nerve; communicating branches

INTRODUCTION

The brachial plexus innervates muscles, joints,and skin of the upper limb by means of supraclavic-ular and infraclavicular branches. The latter comefrom the lateral, medial, and posterior cords of thebrachial plexus. The lateral cord gives rise to the lat-eral root of the median nerve, the lateral pectoralnerve, and the musculocutaneous nerve. The axonsforming the 2 mm in diameter musculocutaneousnerve can be traced back to the spinal nerves C5,C6, and C7 (Buch-Hansen, 1955; Standring, 2004).

The course of the musculocutaneous nerve (MC)is traditionally described as follows: After a 6.7 6 1.6cm distance from its origin (Macchi et al., 2007), itpierces the coracobrachialis muscle and descendslaterally in between the biceps brachii and brachialismuscle. It supplies the coracobrachialis before thenerve enters the muscle. Branches to the biceps bra-chii and brachialis are supplied after the MC haspierced the muscle, approximately 14.1 6 1 cm fromits origin (Macchi et al., 2007). In the elbow, it perfo-rates the deep fascia lateral to the tendon of bicepsand continuous as the lateral cutaneous nerve of

the forearm (Testut and Latarjet, 1954; Standring,2004).

The relationship in between the MC and the cora-cobrachialis muscle was first observed by the Italiananatomist Giulio Casserio (1556–1616), pupil of Fab-ricius and teacher of William Harvey (1578–1657) atPadua (Diab, 1999; Lee, 2000). Subsequently, thenerve has also been known as nervus perforans Cas-serii or perforating nerve of Casserius (Testut andLatarjet, 1954; Diab, 1999).

Variations in the musculocutaneous nerve havebeen discussed and classified by various authors (LeMinor, 1990; Kosugi et al., 1992; Yang et al., 1995;Venieratos and Anagnostopoulou, 1998; Choi et al.,

*Correspondence to: Roberto Andres Guerri-Guttenberg, Depart-ment of Anatomy, Facultad de Ciencias Biomedicas, Hospital Uni-versitario Austral Juan Domingo Peron 1500, Pilar, Buenos AiresB1664INZ, Argentina. E-mail: [email protected]

Received 15 January 2009; Revised 26 March 2009; Accepted3 June 2009

Published online 27 July 2009 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/ca.20828

VVC 2009 Wiley-Liss, Inc.

Clinical Anatomy 22:671–683 (2009)

Page 2: Classifying musculocutaneous nerve variations

2002; Loukas and Aqueelah, 2005). The most fre-quently reported variants include the presence ofcommunicating branches with the median nerve, thenerve not perforating the coracobrachialis muscle(CB) and less frequently its absence (Sunderland,1978; Krishnamurthy et al., 2007; Uysal et al., 2009).

The aim of this study is to (1) describe variationsof the musculocutaneous nerve in fetuses and adultcadavers, (2) identify problems in current classifica-tions and propose a new one, and (3) to discuss clin-ical manifestations of isolated MC injury with andwithout the presence of anatomical variations.

MATERIALS AND METHODS

Thirteen adult cadavers and 15 human fetusesfrom the Anatomy Department of the Austral Univer-sity were included in this study. This study has beenapproved by the ethics committee of the Austral Uni-versity Hospital. A total of 30 upper limbs of humanfetuses and 26 upper limbs of adult cadavers (n ¼56) were dissected. Standard dissection techniqueswere used to expose the brachial plexus. For thispurpose, in most fetuses blood vessels and the clavi-cle were removed. Variations found in the musculo-cutaneous nerve were recorded. Gestational age wascalculated using fetal foot length measurement(Drey et al., 2005).

Statistical analysis was performed using GraphPadPrism1 v5.0 and Microsoft Excel1. The incidence ofanatomical variations of the MC occurring in fetuseswas compared with those found in adult cadavers.The same analysis was performed to compare itsoccurrence in right versus left upper limbs. For allanalyses, Fisher’s exact test was used.

A systematic review of the literature was per-formed in MEDLINE index using the following searchalgorithm: ‘‘Musculocutaneous Nerve’’ [MeSH MajorTopic]. The search was extended to the SciELOindex. Articles were selected for review if one of thefollowing aspects was discussed: (1) classificationsand (2) anatomical variations.

RESULTS

In 3.6% of the limbs (two out of 56; one adult,one fetus), the MC was absent (Figs. 1 and 2). In43% of the dissected limbs (24 out of 56; 14 adults,10 fetuses), there were no communications inbetween the MC and the median nerve (Classicdescription). In 43% (24 out of 56; six adults, 18fetuses), there was one communication in betweenboth nerves (Figs. 3 and 4), and in 10.7% (six out of56; five adults, one fetus) there were two (Fig. 5).The direction of the communications was alwaysfrom the MC to the median nerve except in two limbs(one adult, one fetus) of double communications inwhich one of them was in the opposite direction(Figs. 5 and 6). Eighty-four point 6% of the commu-nications were proximal to the point where the MCpierces the coracobrachialis muscle, 7.7% were dis-tal, and 7.7% had one proximal and one distal com-municating branch.

In 1.8% of the limbs (one out of 56; one fetus), adistal origin of the median and musculocutaneousnerves was found (Fig. 7). In this dissection, it canbe seen how the lateral cord pierces the coracobra-chialis muscle and then gives rise to the MC and lat-eral root of the median nerve.

In 11.1% of the limbs where the MC was present(six out of 54; five adults, one fetus), the nerve didnot pierce the CB (Fig. 6). In one limb (Fig. 2), com-munications in between the lateral and medial cordswere found.

Two-sided Fisher’s exact test revealed no signifi-cant difference when comparing the occurrence ofthe following anatomical variations of the MC infetuses versus adult cadavers: Presence of commu-nications in between MC and median nerve (P ¼0.1700), distal versus proximal communications (P ¼

Fig. 1. Fetus: age 23 weeks. Type 0-1 (0- MCabsent, 1- all branches to coracobrachialis, biceps bra-chii, brachialis and the lateral cutaneous nerve of theforearm originate from a common trunk from the me-dian nerve). Note that other authors may refer to thissame variation as MC fused with median nerve, or evenas MC originating from median nerve. MN, mediannerve; CN, medial antebrachial cutaneous nerve; UN,ulnar nerve; M, Medial cord; L, lateral cord; Mr, medialroot of the median nerve; TD, thoracodorsal nerve; *,Common trunk from the median nerve giving rise tobranches for coracobrachialis, brachialis, biceps brachii,and lateral cutaneous nerve of the forearm. [Color fig-ure can be viewed in the online issue, which is availableat www.interscience.wiley.com.]

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1), MC not perforating coracobrachialis muscle (P ¼0.0862). In addition, no significant difference wasfound when comparing the presence of communica-tions in right versus left upper limbs (P ¼ 0.7089).

DISCUSSION

The musculocutaneous nerve not perforating thecoracobrachialis muscle was found with a frequencyof 11.1%. Correspondingly, Choi et al. (2002) foundit in 7.4% and Chitra (2007) in 6% of the cases.

MC is absent in amphibians, reptiles, and birdswhose muscles of the upper arm are solely inner-vated by the median nerve (Prasada Rao, 2000). Inhuman subjects, the absence of the nerve wasdescribed with a frequency of 6% (Chitra, 2007), 5%(Choi et al., 2002), 1.7% (Beheiry, 2004), and 1.4%(Buch-Hansen, 1955). In our study, we found twocases of absence of MC comprising 3.6% of the dis-sections. On the other hand, Arora and Dhingra(2005) reported this variation in 15 out of 100

cadavers. Further cases of MC absence have beenreported by Ihunwo et al. (1997), Sud and Sharma(2000), Prasada Rao et al. (2001), Jahanshahi et al.(2003), and Nayak (2007). Interestingly, the casereported by Aydin et al. (2006) bares great similaritywith our dissection seen in Figure 2. Both show theabsence of the MC (Type 0–2, see proposed classifi-cation) with a nerve connection between the lateraland medial cords.

Communicating branches are usually interpretedas fibers that should have run through the lateralroot of the median nerve and failed to do so, butentered the MC and joined the nerve later (PrasadaRao, 2000). The presence of communications inbetween the MC and median nerve reported in theliterature was of 10% by Uysal et al. (2009), 13.9%by Venieratos and Anagnostopoulou (1998), 16% byKrishnamurthy et al. (2007), 20% by Kwolczak-McGrath et al. (2008), 21% by Choi et al. (2002),24% by Meals and Calkins (1991), 26% by Chitra(2007), 31.3% by Olave et al., (2000), 33% by Pra-sada Rao (2000), 36% by Eglseder and Goldman

Fig. 3. Fetus: age 20 weeks. Type 1-A-1-P (1-MCpresent, A- MC pierces coracobrachialis, 1-one commu-nication, P-communication is proximal to coracobrachia-lis). MC, musculocutaneous nerve; CB, coracobrachialismuscle; MN, median nerve; CN, medial antebrachial cu-

taneous nerve; UN, ulnar nerve; Lr, lateral root of themedian nerve; C, communication; RN, radial nerve.[Color figure can be viewed in the online issue, which isavailable at www.interscience.wiley.com.]

Fig. 2. Adult cadaver. Type 0-2 (0- MC absent, 2-branches to CB, BB, B and LCN originate from a maintrunk of the median nerve). L, lateral cord; M, medialcord; Mr, medial root of median nerve; MN, mediannerve; UN, ulnar nerve; White arrows, branches origi-

nating from the median nerve itself; Orange arrow,nerve connection between the lateral and medial cords.[Color figure can be viewed in the online issue, which isavailable at www.interscience.wiley.com.]

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Fig. 4. Fetus: age 21 weeks. Type 1-A-1-D (1- MCpresent, A- MC pierces coracobrachialis, 1- one commu-nication, D- communication is distal to coracobrachia-lis). MC, musculocutaneous nerve; CB, coracobrachialismuscle; MN, median nerve; CN, medial antebrachial cu-

taneous nerve; UN, ulnar nerve; Lr, lateral root of themedian nerve; Mr, medial root of the median nerve; C,Communication; AA, axillary artery; BA, brachial artery.[Color figure can be viewed in the online issue, which isavailable at www.interscience.wiley.com.]

Fig. 5. Fetus: age 20 weeks. Type 1-A-2-PD (1- MCpresent, A- MC pierces coracobrachialis, 2- two commu-nications, PD- One proximal and one distal communica-tion). The box shows the proximal communication froma different perspective. MC, musculocutaneous nerve;

MN, median nerve; CN, medial antebrachial cutaneousnerve; Lr, lateral root of the median nerve; C, commu-nication; Mr, medial root of the median nerve. [Colorfigure can be viewed in the online issue, which is avail-able at www.interscience.wiley.com.]

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(1997), and 41.5% by Vallois (Le Minor, 1990). Inthe current study, it was found with a frequency of53.6%. On the other hand, Bergman et al. (1988)reported that communications with median nerveusually occur in the lower third of the arm with a fre-quency, in this region, of 8%. Kosugi et al. (1992)found that the frequency of communications incadavers with supernumerary heads of the bicepsbrachii was of 54.7% while a previous study of thisgroup (Kosugi et al., 1986) performed in cadaverswithout this variation was of 21.8%. Consequently,they postulated that the presence of a supernumer-

ary head influences the branching pattern andcourse of the MC (Kosugi et al., 1992).

The relationship of communications with the pointof entry of the MC into coracobrachialis muscle wereproximal in 33% (Choi et al., 2002), 41% (Venier-atos and Anagnostopoulou, 1998), 70% (Chitra,2007), 81.4% (Kosugi et al., 1992), and 84.6% inour study. They were distal in 30% (Chitra, 2007),45% (Venieratos and Anagnostopoulou, 1998), 65%(Choi et al., 2002), and 7.7% in the our study. Uysalet al. (2003) found a distal communication in twoout of 200 limbs of aborted fetuses. Both proximal

Fig. 6. Adult cadaver. Type 1-B-2 (1- MC is pres-ent, B- MC does not pierce coracobrachialis muscle, 2-Two communications are present). Lr, lateral root of themedian nerve; Mr, medial root of the median nerve;MC, musculocutaneous nerve; MN, median Nerve; AA,

axillary artery; white arrow, communication from theMC to the median nerve; orange arrow, communicationfrom the median nerve to the MC. [Color figure can beviewed in the online issue, which is available at www.interscience.wiley.com.]

Fig. 7. Fetus: age 18 weeks. Type 1-A-4 (1-MCpresent, A- Lateral cord pierces coracobrachialis, 4-Dis-tal origin of median nerve and MC). The clavicle hasbeen removed to expose trunks of the brachial plexus.st, superior trunk; it, inferior trunk; mt, middle trunk;M, medial cord; P, posterior cord; L, lateral cord; Lr, lat-eral root of the median nerve; Mr, medial root of the

median nerve; MC, musculocutaneous nerve; CB, cora-cobrachialis muscle; MN, median nerve; UN, ulnarnerve; RN, Radial nerve; OM, omohyoid muscle; whitearrow, point where the MC originates; orange arrow,point where the median nerve originates. [Color figurecan be viewed in the online issue, which is available atwww.interscience.wiley.com.]

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and distal communications were found in 2% (Choiet al., 2002) and 7.7% in this article.

In the present study, except two limbs, all com-munications went from the MC to the median nerve.Olave et al. (2000) described communication in theopposite direction in one out of 36 dissections, Chiar-apattanakom et al. (1998) found it in five out of 112cases/limbs, and Meals and Calkins (1991) reportedit occurring in 2% of the cases.

Because of anatomical findings reported in dogs,monkeys and some apes it has been suggested thatthese communications may represent a primitivenerve supply of the anterior arm muscles (Aroraet al., 2003; Prasada Rao, 2000).

Current Classifications

Seven ways to classify variations in the musculo-cutaneous nerve have been published, some ofwhich were modified or extended by other authorswho could not classify their findings with current tax-onomies (Sunderland, 1978; Le Minor, 1990; Kosugiet al., 1992; Yang et al., 1995; Venieratos and Ana-gnostopoulou, 1998; Choi et al., 2002; Loukas andAqueelah, 2005).

Sunderland (1978) arranged MC variations in thefollowing groups. (1) Variations in the origin of theconstituent nerve fibers. (2) Variations in relation tothe muscle of the arm. (3) Variations in relation tothe median nerve, and (4) Variations in distribution.

Le Minor (1990) classified the MC variations intofive types. Type I: No communication is present inbetween the MC and the median nerve. The MC per-forates the coracobrachialis and sends motorbranches to innervate the coracobrachialis, bicepsbrachii and brachialis muscles. This qualifies as theClassic description found in textbooks. Type II: Agroup of fibers leave the MC to connect with the me-dian nerve. This corresponds to a communication inbetween the MC and the median nerve that may besimple, multiple or plexiform. Type III: All fibersfrom the lateral root of the median nerve accompanythe MC. This qualifies as the lateral root of the me-dian nerve originating from the musculocutaneousnerve. A low origin of the median nerve results fromthis disposition. Type IV: All fibers of the MC areassociated with the lateral root of the median nerve.After a certain distance the fibers leave the mediannerve and perforate the coracobrachialis muscle.This disposition is described as musculocutanoeusnerve being detached from the median nerve. TypeV: All fibers of the MC remain associated with the lat-eral root of the median nerve, join the trunk of thenerve and accompany the nerve through its entirecourse. This disposition is described as absence ofmusculocutaneous nerve or as fusion of the muscu-locutaneous nerve with the median nerve.

Kosugi et al. (1992) classified the branching pat-tern of the musculocutaneous nerve into five groups.Group 1: pattern without communication. Group 2: acommunicating branch from the MC to the mediannerve. Group 3: a branch running form the mediannerve to the MC. Group 4: Both the above communi-cations (Groups 2 and 4) were present in the same

limb. Group 5: other patterns. Group 2 was subdi-vided into three subgroups. Subgroup A; the originof the branch was before the musculocutaneousentered the coracobrachialis. Subgroup B; the com-municating branch passed through the muscle. Sub-group C: the communicating branch originated afterthe nerve exited the muscle. This last subgroup wasfurther divided into two divisions according to thepoint of the communicating branch: before, or afterthe branch to the biceps brachii were given off.

Yang et al. (1995) classified the distribution ofmotor fascicles to biceps and brachialis. The innerva-tions pattern of the biceps was divided into threetypes. Type I: a primary motor branch bifurcatesinto two secondary nerve branches, each separatelyinnervating the long and short heads of the biceps.Type II: two primary motor branches from the mainmusculocutaneous nerve trunk. The proximal branchinnervates the short head of the biceps and the distalbranch innervates the long head of the biceps. TypeIII: primary motor branch from the main musculocu-taneous nerve trunk that bifurcates into two second-ary branches to individually innervate the two headsof the biceps, plus an additional primary branch, dis-tal to the former that innervates the distal part ofthe biceps at its common belly.

The innervations pattern of the brachialis musclewas divided into two types. Type I: Single primarybranch innervating the brachialis from the mainmusculocutaneous nerve trunk. Type II: two primarybranches that innervate the brachialis from the mainmusculocutaneous nerve trunk.

Venieratos and Anagnostopoulou (1998) classifiedcommunications in between the MC and mediannerve in relation to the point of entry of the MC intocoracobrachialis. Type I: Communications wereproximal. Type II: Communications were distal tothe muscle. Type III: The MC does not pierce thecoracobrachialis.

Choi et al. (2002) described three patterns of con-nections between the MC and the median nerve. Pat-tern 1: Fusion of MC and median nerves. Pattern 2a:Single connecting branch between the musculocuta-neous and median nerves. Pattern 2b: Two or threebranches from the MC joining to form one anasto-motic branch to the median nerve. Pattern 3: Twoconnecting branches between the median and mus-culocutaneous nerve were present.

Loukas and Aqueelah (2005) extended Venieratosclassification by adding an additional type: Type IV;Communications were proximal to the point of entryof the MCN into the coracobrachialis and an addi-tional communication took place distally.

Problems Concerning CurrentClassifications

Anatomists may find it hard to classify their find-ings using only one of the current classifications. Inaddition, the absence of clear definitions in currentclassifications leads to problems such as having threenomenclatures for one same anatomical variation.

What several authors name as absence of muscu-locutaneous nerve (Gumusburun and Adiguzel,

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2000) other refer to as musculocutaneous nervefused with median nerve (Choi et al., 2002) or evenas musculocutaneous nerve originating from mediannerve (Bergman et al., 1988). In our opinion, toavoid confusions the term fusion should berestrained to the cases in which the nerve is identi-fied separately in its origin but afterwards adheres tothe median nerve [Fig. 9, illustration 4, also seereference (Song et al., 2003)].

This problem extends to other variations. Authorslike Saeed and Rufai (2003), and Eglseder andGoldman (1997) consider that if communicationsjoined the median nerve in the upper third of thearm they are regarded as additional lateral roots.Other authors such as Venieratos and Anagnosto-poulou (1998), Choi et al. (2002), and Chitra (2007)classified as proximal communications what the pre-vious authors considered double roots. Alternatively,Buch-Hansen (1955) stated that if the distal root isthicker than the proximal it is considered a secondlateral root of the median nerve, but when it is thin-ner it is referred to as a communicating branch.

A reader not familiarized with this problem maymisinterpret reported frequencies of this variation.For example, Eglesder and Goldman (1997) reportedcommunications appearing in 36% of the cases whilethe current article found it in 53.6%. As theseauthors consider proximal communications as addi-tional lateral roots the percentage represents distalcommunications only. To compare these results withthis article, the reader should add 36% (distal com-munications) to 14% which is similar to the fre-quency of double lateral roots (proximal communica-tions) reported by the author.

Another example of this problem can be identifiedin publications where duplicated musculocutaneousnerves were reported (Abu-Hijleh, 2005; Abhayaet al., 2006). In both cases, the distal musculocuta-neous nerve continued as the lateral cutaneousnerve of the forearm. Nevertheless, given that thenerve arose from the median nerve, it could beregarded as an anomalous innervations pattern ofthe median nerve rather than as a duplicated MC.

The lack of a classification dealing with most var-iations with clear definitions to avoid ambiguityexplains the current difficulty in comparing resultswith other authors.

Proposed Classification

To solve these problems, the following classificationis proposed. To classify the musculocutaneous nervevariations, a four step algorithm was produced whichassigns numbers and letters at each step (Fig. 8).

First step: To determine the presence or absenceof the MC

0. MC is absent (3.6%). Absence of the musculo-cutaneous nerve is defined as the anatomicalvariation occurring when all fibers from the lat-eral cord of the brachial plexus remain associ-ated with the lateral root of the median nerve(Figs. 1 and 2).

1. MC is present (96.4%) MC is defined as thenerve that originates from the lateral cord of

the brachial plexus at the point where the lat-eral root of the median nerve is detached fromit (Figs. 3–5 and 7).

Second step (when the MC is present): Todetermine if the MC pierces the coracobrachialismuscle

A. The MC perforates the coracobrachialis muscle(88.9%; Fig. 4).

B. The MC does not perforate the coracobrachialismuscle (11.1%; Fig. 6).

Third step (Fig. 9): To determine the presenceof communications in between the MC and the me-dian nerve or other variations

0. No communications are present (43%; Classicdescription found in textbooks).

1. One communication is present (43%; Figs. 3and 4).

2. Two or more communications are present(10.7%; Figs. 5 and 6).

3. The MC joins with the median nerve (Songet al., 2003).

4. Distal origin of the MC (1.8%; Fig. 7).

In this case, the lateral root of the median nerveis detached from the lateral cord below the axilla.According to the above definition, this would meanthat the MC has a distal origin. The median nervewill also have a distal origin considering that the lat-eral root would be joining the medial root below theaxilla as well. In these cases, it is evident that theMC given its low origin will not perforate the CB. Forthis reason letter A assigned in the second step ofthe classification should be interpreted as the lateralcord perforating the coracobrachialis muscle. Anexample of 1-A-4 is illustrated in Figure 7 and in thecase report of Abhaya et al. (2003). Refer to Nayaket al. (2006) for an example of a 1-B-4.

Fourth step (Fig. 10): To determine the rela-tionship of the communications between the MC andthe median nerve with the point of entry of the MCinto coracobrachialis muscle

P. Communications are proximal to the point ofentry of the MC into coracobrachialis(84.6%;Fig. 3).

D. Communications are distal to the muscle(7.7%; Fig. 4).

PD. Communications are both proximal and dis-tal (7.7%; Fig. 5).

Second step in case the MC is absent (Fig.11): To determine the disposition of the motorbranches that innervate the coracobrachialis, bicepsbrachii and brachialis muscles, and the sensorybranch that innervates the lateral forearm.

1. Branches originate from a common trunk aris-ing from the median nerve (1.8%; Fig. 1).

2. Branches originate from the median nerve itself(1.8%; Fig. 2).

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We believe that this taxonomy succeeds in com-bining preexisting classifications into an integratedand more detailed one. Nevertheless, to avoid com-plicating the classification some variations with avery low frequency were excluded. For example,though clinically important, the direction of the com-munications is not included in the proposed classifi-cation. Similarly, the plexiform pattern of communi-cations was also omitted.

Clinical Importance

Though uncommon, isolated lesions of the MChave been reported with increasing frequency. Themechanism of atraumatic lesions can be divided intoproximal involving the entire nerve and distal whenonly the lateral cutaneous nerve is affected.

In the first group, the causes were reported to beentrapment syndromes at the level of the coracobra-

Fig. 8. Classification of the musculocutaneousnerve variations. First step (Black boxes): identifythe presence or absence of the MC. Second step(green boxes); identify if MC pierces coracobrachialis.In case of MC absent; to identify disposition of branchesfor coracobrachialis (CB), biceps brachii (BB), brachialis(B) and lateral cutaneous nerve of the forearm (LCN).

Third step (Red boxes); identify communications orother variations. Fourth step (Blue boxes); identifythe relationship of communications to the point of entryof MC into coracobrachialis. f: figure number. [Color fig-ure can be viewed in the online issue, which is availableat www.interscience.wiley.com.]

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chialis (Papanikolaou et al., 2005) as well as inbetween the biceps brachii and brachialis muscle(DeFranco and Schickendantz, 2008). In thesecases, the lesion results from compression or trac-tion. Compression can be caused either by vigorouscontractions after strenuous physical activity (Simo-netti, 1999) or by chronic pressure secondary tohyperthropy (Fattal et al., 1998) as it occurs in

weight lifters, leading to direct mechanical and ische-mic injury to the nerve with subsequent focal demy-elination and variable axonal degeneration (Papani-kolaou et al., 2005). Mass lesions should also beconsidered in patients with atraumatic MC neuropa-thies. Accordingly, Juel et al. (2000) found a proxi-mal humeral osteochondroma to be the cause of anisolated MC lesion in a 22-year-old patient.

Fig. 9. Third step of classification: 0- No communi-cations between MC and median nerve. 1- One commu-nication. 2- Two or more communications. 3- MC joinsmedian nerve. 4- Distal origin of MC and median nerve.L, lateral cord; M, medial cord; MC, musculocutaneousnerve; CB, branch to coracobrachialis; BB, branch tobiceps brachii, B, branch to brachialis; LCN, lateral cuta-

neous nerve; MN, median nerve; UN, ulnar nerve; Lr,Lateral root of the median nerve; Black arrow, lateralroot of the median nerve; Orange arrows, communica-tions; Green arrows, MC joining with median nerve.[Color figure can be viewed in the online issue, which isavailable at www.interscience.wiley.com.]

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Fig. 11. Second step in case of MC absent: 1- allbranches to coracobrachialis, biceps brachii, brachialisand the lateral cutaneous nerve of the forearm originatefrom a common trunk from the median nerve. 2- allbranches originate from the median nerve separately.L, lateral cord; M, medial cord; P, posterior cord; CB,

branch to coracobrachialis. BB, branch to biceps brachii;B, branch to brachialis; LCN, lateral cutaneous nerve ofthe forearm.MN, median nerve; UN, ulnar nerve. [Colorfigure can be viewed in the online issue, which isavailable at www.interscience.wiley.com.]

Fig. 10. Fourth step of classification: P: Communi-cation is proximal to the point of entry of MC into cora-cobrachialis. D: Communication is distal to the muscle.PD: One communication is proximal and one distal tothe muscle. L, lateral cord; MC, musculocutaneous

nerve; CB, coracobrachialis muscle; MN, median nerve;UN, ulnar nerve; C, communication. [Color figure canbe viewed in the online issue, which is available atwww.interscience.wiley.com.]

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The traction mechanism of injury is produced due tothe fact that these muscles act like anchorage pointsto the MC. In this way, hyperextension leads to nervestretching. This mechanism was described in a sky-diver due to the arm-shoulder abduction, extensionand external rotation performed during simulated freefall in a vertical wind-tunnel (Mautner and Keel,2007). Extensive stretching may also occur due to animproper arm positioning during sleep (Inaba andYokota, 2003) or throughout surgical procedures(Ewing, 1950; Dundore and DeLisa, 1979). Further-more, a case was described occurring in a fast-pitchsoftball player where the mechanism was described asa combination of stretching due to the circumductionmotion and compression between biceps brachii andbrachialis due to strong muscular contraction to con-trol elbow during pitching (DeFranco and Schicken-dantz, 2008). Other cases of isolated musculocutane-ous nerve injury have occurred during, rowing, using asledge hammer, football throwing, and repetitive car-rying of a heavy rolled object also known as Carpetcarrier’s palsy. (Sander et al., 1997; Inaba andYokota, 2003; Papanikolaou et al., 2005).

Distal mechanisms include entrapment syndromesin the superficial antebrachial fascia (Belzile andCloutier, 2001) and the biceps tendon (Gillinghamand Mack, 1996). Iatrogenic injury of the lateralcutaneous nerve of the forearm has been reported tooccur in five out of 50 patients with humeral shaftdisplaced fractures after treatment with Russel-Tay-lor interlocked nerves (Blyth et al., 2003). Gardneret al. (2005) determined the location of a dangerzone (12.2–14.8 cm distal to the greater tuberosityalong the medial border of the humeral shaft) wherethe MC could be injured during helical plating of theproximal humerus as a consequence of percutaneousscrew placement. Idiopathic neuralgic amyotrophy, arare disorder of unknown etiology may also affectthe musculocutaneous nerve (Rix et al., 2006)though it is not its typical presentation.

Clinical manifestations depend on two factors; thelocation of the injury and presence of anatomicalvariations. In a MC with no variations (1-A-0), aproximal lesion would cause a mixed motor and sen-sory syndrome clinically identified as marked weak-ness of elbow flexion, and sensory impairment in thedistribution of the lateral cutaneous nerve of theforearm. On the other hand, distal lesions causepure sensory findings identified as pain over the an-terolateral aspect of the elbow, burning dysesthesiaof the lateral forearm, and accentuation of symp-toms by elbow extension and forearm pronation (Gil-lingham and Mack, 1996).

In cases of MC variations such as 1-A-1-D (Fig. 4)where a distal communication is present, proximalinjuries of the MC would also involve median nervefibers. Similar clinical findings may be expected if aproximal injury occurs in the presence of a variationsuch as 1-A-4 (Fig. 7), where the lateral cord is foundto pierce the coracobrachialis and a distal origin of theMC is present. In cases of 1-A-1-P, Saaed and Rufai(2003) have postulated that due to the intimate rela-tionship of the proximal communication with the axil-lary artery, compression leading to ischemic pain or

variable arterial insufficiency during certain posturalmaneuvers of the shoulder joint may occur.

Though rare, communications may have an oppo-site direction (Fig. 5). In these cases, a proximallesion of the median nerve would also involve MCfibers, while a proximal lesion of the MC would stillpreserve some functions of this nerve. Where thereare two communications at the same level but withdifferent directions (Fig. 6) one could speculate that acomplete proximal lesion in either of the two nerveswould result in an incomplete loss of function in bothnerves. The figure also illustrates the high risk of iat-rogenic damage to these communications that couldoccur in an anterior surgical approach during retrac-tion for exposure of fracture line (Canter et al., 2005).

Lesions of the median nerve in cases where theMC is absent (Figs. 1 and 2) would also lead to unex-pected clinical signs. In these cases signs of mediannerve and MC injury would coexist. Appreciation ofthese anatomical variations is also important in re-gional anesthesia. Orebaugh and Pennington (2006)described a case of a patient who underwent axillarynerve block for a wrist arthroscopy procedure withreal-time ultrasound and peripheral nerve stimulatorguidance. The median nerve located with ultrasoundresponded to the stimulating needle with strongbiceps contraction and forearm pronation. The ultra-sound showed no neural structure that could repre-sent the musculocutaneous nerve in its usual posi-tion (Orebaugh and Pennington, 2006), revealing thecause of this unusual response to be the MC ab-sence.

The difficulty in correctly identifying the anatomi-cal variation responsible of the anomalous innerva-tion patterns of the upper extremity can be illus-trated with the following case presented by Mealsand Calkins (1991). A 28-year-old man was stabbedwith a small screwdriver in the proximal medial as-pect of his arm. In addition to a complete motor andsensory deficit of the median nerve he presentedincapacity to contract biceps brachii or brachialismuscle. According to Song et al. (2003), MC absencewould explain these symptoms. Nevertheless, if weassume that the MC lesion was incomplete (e.g.,preserved function of the lateral cutaneous nerve ofthe forearm) a distal communication from themedian nerve to the MC could also explain thesesymptoms.

These rarely diagnosed conditions should be partof every differential diagnoses for peripheral nerveentrapment syndromes in the upper extremity (Bel-zile and Cloutier, 2001).

The classification should help to clarify the confu-sion resulting from the use of multiple terms todescribe one same anatomical variation. In return,being familiarized with these variations will avoidmisinterpreting clinical symptoms.

ACKNOWLEDGMENTS

The authors would like to thank our friends Maxi-miliano Olivera, Marıa Laura Picoletti, and MarcosCabrera for their help.

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