A Possible Accessory Muscle of the Serratus Posterior Superior Muscle

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Case Report A Possible Accessory Muscle of the Serratus Posterior Superior Muscle

Kerrie Lashley 1,* and Guinevere Granite 2

1 Department of Anatomy and Cell Biology, George Washington University, Washington, DC 20037, USA 2 Department of Surgery, Uniformed Services University of the Health Sciences, Bethesda, MD 20814, USA; [email protected] * Correspondence: [email protected]

Abstract: Anatomical variation is defined as the normal range of possibilities in the topography and morphology of body structures. In contrast, an anomaly is any structural or functional anatomical finding beyond the normal range of possibilities. This case study describes a muscular anomaly found in a 73-year-old preserved Caucasian male. We observed a left-sided anomalous muscle originating from the transverse process of the C1 (Atlas) vertebra and inserting onto the proximal attachment of the serratus posterior superior (SPS) muscle at the C7 level. We suggest that this anomaly is a result of early embryological development and hypothesize that the atypical neck muscle may reinforce the action of the SPS. This finding is rare and no reference of it can be found in the literature. Reporting anatomical anomalies is important for the medical literature and education.

Keywords: accessory muscle to serratus posterior superior; muscular anomalies; variations in human myology; anatomical variations

1. Introduction Citation: Lashley, K.; Granite, G. A Muscular variations are common in the human body and are well-documented in Possible Accessory Muscle of the the literature. These variants occur within the normal range of possibilities that may be Serratus Posterior Superior Muscle. comprised of morphometric changes, supernumerary elements, consistency and spatial Reports 2021, 4, 2. https://doi.org/ orientation [1,2]. Muscular anomalies are much rarer, and anatomists observe them dur- 10.3390/reports4010002 ing routine cadaveric dissection or surgeons discover them inadvertently during surgical procedures [3]. Anomalies are typically asymptomatic and may go unnoticed during the in- Academic Editor: Eustace Johnson dividual’s life. With the development of non-invasive imaging techniques and the increase Received: 7 January 2021 in cadaveric studies, however, anatomic anomalies are being detected more frequently [2]. Accepted: 21 January 2021 Published: 25 January 2021 In this case study, we observed a rare unilateral anomalous muscle in the left posterior neck of a human cadaver. It was located deep to the rhomboid muscles and coursed superior and medial to the serratus posterior superior (SPS) muscle. In addition, we Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in found differences in the cervical origins of the right and left levator scapulae muscles published maps and institutional afﬁl- (LSMs), resulting in muscular asymmetry in this individual. This anomalous muscular iations. development is uncommon, and we were unable to ﬁnd a description of such a case in the literature. Therefore, it is important to provide a detailed description of this rare anomalous muscle.

2. Materials and Methods Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. During cadaveric dissection, we detached the superficial extrinsic back muscles, in- This article is an open access article cluding the trapezius, latissimus dorsi, and the rhomboid muscles from their proximal distributed under the terms and attachments and reflected them. The levator scapulae muscle was not reflected. This conditions of the Creative Commons exposed the intermediate extrinsic back muscles, including the serratus posterior superior Attribution (CC BY) license (https:// (SPS). We detached the SPS from the spinous processes at the C7-T2 vertebral level. We creativecommons.org/licenses/by/ observed the anomalous muscle during the detachment of the SPS at its proximal attach- 4.0/). ments. Delicate dissection of the anomalous muscle allowed us clear definition and further

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observed the anomalous muscle during the detachment of the SPS at its proximal attach- Reports 2021, 4, 2 ments. Delicate dissection of the anomalous muscle allowed us clear definition2 of 5 and further examination of its attachment sites. We detached the deep intrinsic muscle, the splenius muscle, proximally from the nuchal ligament and spinous processes of C7-T6 verte- examinationbrae. We conducted of its attachment this dissection sites. We bilaterally. detached the deep intrinsic muscle, the splenius muscle, proximally from the nuchal ligament and spinous processes of C7-T6 vertebrae. We3. Case conducted Report this dissection bilaterally. 3. CaseDuring Report routine dissection of the neck and back regions, we found a unilateral anom- alousDuring muscle routine occurring dissection within of the a neck73-year-old and back Caucasian regions, we male found human a unilateral cadaver. anoma- The anom- lousalous muscle muscle occurring originated within from a 73-year-old the left Caucasian transverse male process human of cadaver. the atlas The and anomalous extended inferi- muscleorly to originated insert onto from the the SPS left (Figure transverse 1). The process left of SPS the presented atlas and extended its common inferiorly anatomy: to proxi- insertmal attachments onto the SPS from (Figure the1). spinou The lefts processes SPS presented of C7-T2 its common vertebra anatomy:e and its proximal distal attachments attachmentsto the superior from borders the spinous of processesthe second of C7-T2through vertebrae fifth ribs. and itsThe distal tendinous attachments fibers to theof the anom- superior borders of the second through fifth ribs. The tendinous fibers of the anomalous alous muscle inserted superficially, and slightly perpendicular onto the left SPS proximal muscle inserted superficially, and slightly perpendicular onto the left SPS proximal end. Theend. fused The fused fibers offibers the twoof the muscles two muscles attached attach to theed spinous to the processspinous of process the C7 vertebraof the C7 vertebra (Figure(Figure2). 2). The The anomalous anomalous muscle muscle shared shared a common a common attachment attachment at the transverse at the transverse process process ofof thethe atlas atlas with with the the upper upper portion portion of the of splenius the splenius cervicis cervicis muscle andmuscle two and of the two upper of the upper muscularmuscular slips slips of of the the left left LSM LSM (Figure (Figure2). In2). length,In length, the anomalousthe anomalous muscle muscle measured measured 12.5 12.5cm cmand and 0.65 0.65 cm cm wide wide with with a a consistent consistent width width throughout throughout its muscleits muscle belly. belly.

FigureFigure 1. 1.Overview Overview of theof the Posterior Posterior Intermediate/Deep Intermediate/Deep Neck. Accessory Neck. Accessory Serratus Posterior Serratus Superior Posterior Supe- (ASPS)rior (ASPS) Muscle; Muscle; Atlas transverse Atlas transverse process (C1);process Spinous (C1) process; Spinous of cervicalprocess vertebra of cervical 7 (C7); vertebra Erector 7 (C7); SpinaeErector (ES) Spinae Muscles; (ES)Levator Muscles; Scapulae Levator Muscle Scapulae (LSM); Muscle Scapula (LSM (Scp);); Scapula Serratus (Scp Posterior); Serratus Superior Posterior (SPS)Superior Muscle; (SPS Splenius) Muscle; capitis Splenius (Sct) Muscle; capitis Splenius (Sct) Muscle; cervicis Splenius (Scr) Muscle. cervicis (Scr) Muscle.

InIn combination combination with with this this rare rare ﬁnding, finding, there werethere some were noteworthy some noteworthy differences differences in the in the cervical origins of the left LSM compared to the right. The left sided LSM exhibited four cervical origins of the left LSM compared to the right. The left sided LSM exhibited four main muscular slips with distal attachments to the superior angle of the scapula but varied inmain the numbermuscular of muscularslips with slips distal and attachments cervical origins. to the The superior observed angle variabilities of the ofscapula the left but varied LSMin the are number as follows: of muscular (1) muscular slips slips and 1 and cervical 2 shared origins. a common The observed cervical origin variabilities at C1; (2) of the left theLSM third, are broaderas follows: muscular (1) muscular slip, bifurcated slips 1 midway, and 2 shared with one a common muscular cervical slip of cervical origin at C1; (2) originthe third, at C3 broader and the othermuscular at C4; slip, and(3) bifurcated the fourth midway, muscular slipwith originated one muscular from C5; slip no of cervical LSMorigin muscle at C3 slips and originated the other from at C4; C2 (Figureand (3)3A). the The fourth right-sided muscular LSM slip had fouroriginated muscular from C5; no slipsLSM that muscle originated slips originated from the transverse from C2 processes (Figure 3A). of C1–C4 The right-sided vertebrae, respectively, LSM had four and muscular slips that originated from the transverse processes of C1–C4 vertebrae, respectively, and were relatively consistent in size and shape (Figure 3B). The muscular asymmetry in the present case produced a five-headed left LSM and a four-headed right LSM.

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Reports 2021, 4, x FOR PEER REVIEW 3 of 5 were relatively consistent in size and shape (Figure3B). The muscular asymmetry in the present case produced a ﬁve-headed left LSM and a four-headed right LSM.

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FigureFigure 2. 2.Origin Origin and and Insertion Insertion Sites Sites for ASPS. for ASPS. The dashed The dashed line illustrates line illustrates the slightly the perpendicular slightly perpendicular Figure 2. Origin and Insertion Sites for ASPS. The dashed line illustrates the slightly perpendicular insertioninsertion of of the the ASPSinsertion ASPS onto onto of the the proximalthe ASPS proximal onto portion the portion proximal of the SPS.of portion the Asterisks SPS. of the Asterisks SPS. indicate Asterisks theindi upper cateindicate the tendinous the upper upper tendinous tendinous connectionconnection of of the theconnection SPS SPS traveling traveling of the deep SPS deep traveling to the to the ASPS. deep ASPS. Accessoryto the Accessory ASPS. Serratus Accessory Serratus Posterior Serratus Posterior Superior Posterior Superior (ASPS) Superior (ASPS) (ASPS) Muscle;Muscle; Atlas Atlas transverse transverseMuscle; processAtlas process transverse (C1); (C1); Spinous process Spinous process (C1); procSpinous of cervicaless procof vertebracervicaless of cervical 7vertebra (C7); vertebra Serratus 7 (C7); 7 Posterior(C7); Serratus Serratus Poste- Poste- Superiorrior Superior (SPS) Muscle;(SPSrior )Superior Muscle; Splenius (SPS Splenius capitis) Muscle; (Sct) capitis Splenius Muscle; (Sct capitis Splenius) Muscle; (Sct Cervicis) Muscle; Splenius (Scr) Splenius Cervicis Muscle. Cervicis (Scr) (Scr) Muscle. Muscle.

Figure 3. FigureA and 3.3B:A Bilateral and 3B: Asymmetry. Bilateral Asymmetry. (A) Illustrates (A left-sided) Illustrates variations left-sided in LSM variations anatomy. in LSMDifferences anatomy. in cervical origins ofDifferences the five muscular in cervical slips of origins the left of LSM. the ﬁve Shared muscular vertebral slips origin of the of leftLSM LSM. upper Shared slips 1 vertebral and 2, distal origin bifurcation of of middle slip producing slips 3 and 4 with different cervical origins, no muscular slip originating from C2 (*). (B ) Illustrates LSM upper slips 1 and 2, distal bifurcation of middle slip producing slips 3 and 4 with different Figure 3. A and 3B:common Bilateral anatomy Asymmetry. of right sided (A) LSM.Illustrates Four muscular left-sided slips variations of the LSM in with LSM no anatomy.variation in Differencescervical origins. in Accessorycervical Serratus Posteriorcervical origins,Superior no (ASPS) muscular Muscle slip; Atlas originating transverse from process C2 (*). (C1); (B) IllustratesTransverse common processes anatomy of cervical of vertebrae right 2–5 origins of the five muscular(C2-5) Spinoussided slips LSM.process of the Four ofle ftcervical muscular LSM. vertebra Shared slips of 7(C7);vertebral the LSM Levator with origin Scapulae no variationof LSM Muscle u inpper cervical(LSM slips) which origins. 1 and includes Accessory 2, distal the Levatorbifurcation Serratus Scapulae of middle slip producingMuscle slips SlipsPosterior 3 and 1–5; Serratus4 Superiorwith different Posterior (ASPS) Superiorcervical Muscle; (SPS origins, Atlas) Muscle; transverse no musculSplenius process arcapitis slip (C1); (Sctoriginating Transverse) Muscle; Splenius from processes C2 Cervicis (*). of ( cervicalB )(Scr Illustrates) Muscle. common anatomy of right vertebraesided LSM. 2–5 Four (C2-5) muscular Spinous process slips of of th cervicale LSM vertebra with no 7(C7); variation Levator in Scapulaecervical Muscleorigins. (LSM) Accessory Serratus Posterior Superiorwhich (ASPS) includes Muscle the4.; AtlasDiscussion Levator transverse Scapulae process Muscle Slips (C1); 1–5; Transverse SerratusPosterior processes Superior of cervical (SPS) vertebrae Muscle; 2–5 (C2-5) Spinous process of cervicalSplenius vertebra capitis (Sct) 7(C7); Muscle;There Levator are Splenius earlier Scapulae Cervicis reports Muscle (Scr) of supernumerary Muscle. (LSM) which and includes divergent the muscular Levator slips Scapulae of the LSM Muscle Slips 1–5; Serratus Posterior Superiorwith (SPS varying) Muscle; cervical Splenius origins capitis and insertions (Sct) Muscle; [4]. However, Splenius these Cervicis descriptions (Scr) Muscle. always illustrated muscular or tendinous connections to the scapula and were characterized as devi- 4. Discussionant or rogue slips of the LSM. These deviant slips of the LSM fall within the normal range of possibilities and are true variants of the LSM. In the present case, however, the atypical There are earlier reports of supernumerary and divergent muscular slips of the LSM with varying cervical origins and insertions [4]. However, these descriptions always illustrated muscular or tendinous connections to the scapula and were characterized as deviant or rogue slips of the LSM. These deviant slips of the LSM fall within the normal range of possibilities and are true variants of the LSM. In the present case, however, the atypical

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4. Discussion There are earlier reports of supernumerary and divergent muscular slips of the LSM with varying cervical origins and insertions [4]. However, these descriptions always illustrated muscular or tendinous connections to the scapula and were characterized as deviant or rogue slips of the LSM. These deviant slips of the LSM fall within the normal range of possibilities and are true variants of the LSM. In the present case, however, the atypical muscle, Accessory Serratus Posterior Superior (ASPS), does not have any muscular or tendinous connections to the scapula. Its morphology is distinctly different from previous observations of deviant slips of LSM. Therefore, we consider this ﬁnding to be a true representation of a rare muscular anomaly and not a deviant or variant slip of the LSM. Furthermore, the insertion of the anomalous muscle onto the dorsal surface of the SPS suggests that it may have aided or reinforced the action of the SPS during elevation of the ribs, speciﬁcally the second rib, thus functioning as a possible accessory muscle to SPS. Its insertion does not support its action as an accessory LSM because it cannot elevate or rotate the scapula.

4.1. Embryological Implication of the ASPS Muscle development is a complex and multistep process that involves a series of cellular events of cell fusion, migration and attachment [5]. During myogenesis, myoblasts form into migrating myoﬁbers that are guided towards speciﬁc tendon attachment sites to establish connection with the skeletal system [5]. Errors may occur in migration that alter the attachment of muscle and tendon precursor cells, causing ectopic origins and insertions of muscular slips [6]. Therefore, the presence of the ASPS muscle may be a result of errors in the migration of muscle progenitors or tendinous attachment progenitors at the C1 level [7], due to alterations in the microenvironment through which the cells migrate, or Hox-gene related alterations in the axial identity of the progenitors [8].

4.2. Muscular Variation Bias to One Side of the Body While bilateral symmetry in the body’s topography is a central feature of vertebrate anatomy [9], many studies demonstrate that asymmetry is not uncommon [10]. In the present case, muscular variation biased toward the left side of the body suggests a disturbance during development may have affected the symmetry of the musculoskeletal system. In a recent study by Bang et al., 2015, multiple muscular variations from the neck to the lower extremities primarily on the left side were reported in a single cadaver [6]. They attributed this lack of symmetry to momentary disturbances in the formation of the embryonic somites. Somites, which give rise to the vertebrae, ribs and associated muscles and tendons, arise as bilaterally symmetric, paired blocks of paraxial mesoderm in a developing embryo’s left and right sides [11]. Each somite pair carried a speciﬁc axial identity due to the expression of a unique combination of Hox genes [8]. Interestingly, it has been found in several animal models that asymmetries in left–right somite pairs occur when Retinoic acid (RA) signaling is reduced, leading to developmental delay on one side [11]. These ﬁndings suggest that RA signaling is essential to ensure symmetrical mesoderm segmentation and bilateral symmetry along the left–right axis [11]. We speculate that environmental factor(s) acting during early embryonic development may have disturbed this synchrony, leading to a disturbance in the synchronicity of the left and right sides during somitogenesis, causing muscular variation bias in this individual. One such known disruptor of RA signaling is maternal consumption of alcohol [12].

4.3. Clinical Signiﬁcance Embryonic development of the back and neck muscles is complex. Understanding this process is key to identifying congenital anomalies, diagnosing congenital abnormalities and discerning how and where during development they may occur. Anatomic anomalies and variations of the back and neck may contribute to pathological conditions of these Reports 2021, 4, 2 5 of 5

regions such as myofascial syndrome and the need for radical neck dissection surgery. The presence of the ASPS may pose a challenge to surgeons and could result in erroneous diagnosis as a soft tissue tumor in radiologic evaluations. Hence, reporting is not only important for the medical literature and education, but to also help clarify unknown or controversial clinical presentations in the human body. Moreover, due to a limited medical report, there was no reported medical signiﬁcance related to the anomaly and asymmetry in this individual nor was the cause of death related to our ﬁndings. This case report further supports clinical observations that muscular variations, anomalies and asymmetry can exist simultaneously in an individual and that they may occur more commonly than previously thought.

Author Contributions: Conceptualization, K.L.; investigation, K.L.; writing—original draft prepara- tion, K.L.; visualization, K.L.; writing—review and editing, K.L. and G.G. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: Ethical review and approval were waived for this study, given that the material used in this study is considered as a non-human subject; therefore, ethical approval was waived. Informed Consent Statement: Not applicable. Data Availability Statement: Data sharing not applicable. Acknowledgments: With great respect and honor, we thank our donor and his family for such an incredible gift. We thank Ronald W. Rivenburgh, CIV from the Anatomical Gift Program at USUHS, Osvaldo Bustos, Ayo P. Doumatey, Victor Taylor II and Sally Moody for their guidance, mentorship and appreciated contributions. Special thanks to Mohammed Ashraf Aziz for his unwavering support and inspiration. Conflicts of Interest: The authors declare no conflict of interest. Disclaimer: The opinions or assertions contained herein are the private ones of the authors/speakers and not to be construed as official or reflecting the views of the Department of Defense, the Uniformed Services University of the Health Sciences or any other agency of the U.S. Government.

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