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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 9  |  Issue : 3  |  Page : 82-89

Axillary artery variation: The rule not the exception


1 Mayo Clinic Alix School of Medicine, Scottsdale, AZ, USA
2 Department of Surgery, Division of Plastic and Reconstruction Surgery, Department of Surgery, Mayo Clinic, Scottsdale, AZ, USA
3 Department of Cell Biology and Anatomy, LSUHSC School of Medicine, New Orleans, LA, USA
4 Department of Laboratory Medicine and Pathology, Division of Anatomic Pathology, Mayo Clinic, Scottsdale, AZ, USA

Date of Submission28-Jun-2020
Date of Decision11-Aug-2020
Date of Acceptance23-Sep-2020
Date of Web Publication15-Oct-2020

Correspondence Address:
Natalie R Langley
Mayo Clinic, 13400 E, Shea Blvd, Scottsdale 85259, AZ
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/NJCA.NJCA_32_20

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  Abstract 


Introduction: Anatomic morphology commonly depicted in atlases or textbooks is often emphasized in gross anatomy classrooms; however, considerable variation may be observed in cadavers during dissection, particularly in the vascular system. This study statistically assesses the frequency of the classic versus variant axillary artery branching pattern and compares these observations to the incidence of variation described in the literature. Material and Methods: Axillary artery branching pattern was studied in 62 cadaver limbs. A Chi square goodness of fit test with post hoc analyses on the adjusted standardized residuals was used to evaluate branching patterns. Results: A statistically significant difference existed between the observed and expected frequencies of the classic presentation (P < 0.001). The axillary artery branching pattern exhibited the classic presentation in 17.7% of this sample; 82.3% of the limbs displayed a variant in at least one major axillary artery branch. The lateral thoracic and posterior circumflex humeral arteries were significantly variable branches observed in their textbook locations in 40.3% and 61.3% of cases, respectively. The superior thoracic, thoracoacromial, and subscapular arteries were significantly conserved branches documented in their textbook locations in 97%, 98.3%, and 98.3% of cases, respectively. Discussion and Conclusion: While anatomy educators and students understand that anatomic structure has an inherent range of variability, the classic axillary artery branching pattern students expect to find in cadavers and patients rarely occurs. Educators must present a realistic picture of anatomic complexity and emphasize the clinical and surgical implications of anatomical variation.

Keywords: Anatomic variation, anatomy, axillary artery, dissection, medical education


How to cite this article:
Thiele CM, Thornburg DA, Van Nuland SE, Langley NR. Axillary artery variation: The rule not the exception. Natl J Clin Anat 2020;9:82-9

How to cite this URL:
Thiele CM, Thornburg DA, Van Nuland SE, Langley NR. Axillary artery variation: The rule not the exception. Natl J Clin Anat [serial online] 2020 [cited 2020 Nov 28];9:82-9. Available from: http://www.njca.info/text.asp?2020/9/3/82/298163




  Introduction Top


Gross anatomy courses traditionally reinforce didactic learning in the classroom with experiential learning involving cadavers in a laboratory setting. Learning anatomy is challenging because it requires acquiring a new vocabulary [1] and generating three-dimensional mental images.[2] Medical educators must streamline anatomy into a concise and relevant version of the complex discipline by presenting classic, or typical, anatomy as shown in various textbooks, atlases, and virtual applications. Unfortunately, this conveys an imaginary “standard” of the human body, which medical learners expect to see mimicked in cadaveric specimens and future patients.[3],[4] However, individuals of any species demonstrate fluctuation in anatomic size, form, structure and position, known as normal intraspecific biological variation.[3] While some textbooks acknowledge anatomical variants, medical student learners may not have the opportunity to appreciate the full range, prevalence, and clinical significance of anatomical variants since their observations are limited to a small subset of cadavers. Furthermore, dwindling hours devoted to anatomy instruction in medical school curricula leaves little time to explore biological variation.[5],[6] This problem is exacerbated by standardized computer-generated models and virtual reality platforms that depict “textbook anatomy” and limit exposure to anatomical complexity, variation, and developmental anomalies,[7] an issue with which many anatomy educators are struggling amidst necessary instructional changes due to COVID-19.[8]

Showing typical presentations of anatomical structures, rather than all presentations within the normal range of variation, is a teaching strategy that relies on the clinical relevance of the most frequently depicted morphologies in texts and atlases. However, it is unclear how often these depictions characterize the “typical” or “most frequently seen” presentation. The impetus for this study originated at the Mayo Clinic Alix School of Medicine's (MCASOM) Arizona campus where only 11 of 64 upper limbs exhibited the classically-depicted axillary artery branching pattern. The authors questioned if this branching pattern presented a realistic picture of anatomic complexity to medical learners.

The axillary artery is described classically as the continuation of the subclavian artery as it passes distal to the first rib to traverse the axilla. The axillary artery gives rise to six major branches before becoming the brachial artery at the inferior border of the teres major muscle. The axillary artery is described as being divided into three parts by the pectoralis minor muscle [Figure 1]. The first part of the artery lies medial to the pectoralis minor and gives rise to the superior thoracic artery. Two branches arise from the second part, which is located posterior to the pectoralis minor muscle: The thoracoacromial artery and lateral thoracic artery (LTA). Three branches arise from the third part, located distal to pectoralis minor: The subscapular artery (SSA), anterior circumflex humeral artery (ACHA), and posterior circumflex humeral artery (PCHA). The SSA typically divides into two terminal branches, the circumflex scapular and thoracodorsal arteries.
Figure 1: Illustration of the classic presentation of the axillary artery branches. Shaded area indicates the approximate position of pectoralis minor muscle. Illustration credit: Austin Pena

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This study evaluates the branching pattern of the axillary artery over 2 years of anatomy instruction at MCASOM Arizona to assess the comparability of “textbook” and cadaveric learning. The frequency of the classically-described axillary artery branching pattern was evaluated in a cadaveric sample (n = 32) from the mid-Western United States. The observed morphologies were evaluated statistically to determine if the branching pattern was significantly variant or significantly conserved. We hypothesized that the branching pattern of the axillary artery observed in the cadavers would differ significantly from the classic description. Additionally, the morphology and frequency of the variants were compared to variations reported in the literature, as documented by a thorough literature search and frequency analysis of the data within these reports. This two-pronged approach of a statistical analysis of cadaveric data combined with an analysis of previous reports for comparative purposes presents a comprehensive picture of axillary artery morphology and elucidates if the most frequently-reported variants are actual variations or normal occurrences.


  Materials and Methods Top


Course description

The MCASOM anatomy course employs a variety of teaching methodologies, including lectures, small group learning, and cadaveric dissection. The 7-week course has 120 total contact hours, and 56% of this time (~67 h) is devoted to learning through dissection.[9],[10],[11] At MCASOM Arizona, 50 1st-year medical students complete dissections in groups of 3–4 students on their assigned cadaver. The curriculum emphasizes the importance of dissection in anatomy learning, and students are assessed on dissection quality and completeness.[11] Recognition and understanding of anatomical structures are assessed with a final laboratory practical examination.

Study sample and dissection protocol

A total of 32 cadavers were dissected by 1st-year medical students and anatomy faculty at MCASOM Arizona during the Gross Anatomy/Human Structure and Clinical Anatomy of Invasive Procedures courses. The sample consists of 17 Caucasian females (53%) and 15 Caucasian males (47%) from the mid-Western United States with a mean age of 83.8 ± 10 years. Axillary artery branches were documented bilaterally on 30 cadavers and unilaterally on two cadavers, for a total of 62 limbs. Approval for this study was granted by the Mayo Clinic Biospecimens Subcommittee (proposal #19000378).

Arteries were dissected initially by students during the laboratory session devoted to the axillary artery using instructions provided in Grant's Dissector.[12] More detailed dissections and data collection were completed by faculty after the class session. Branches were identified by one faculty member (SVN or DT) and verified by a second faculty (NRL) prior to documentation via labeled drawings and photographs. Based on the classic description of the six major axillary artery branches, the entirety of the branching pattern was recorded as either “textbook” or “variant.” When variations were encountered in any of the classically-described presentations, they were documented for comparison to the literature and statistical analysis of the variants. The SSA branches (thoracodorsal and circumflex scapular arteries) were documented, as well. [Table 1] describes the criteria used to define the classic presentation of each major branch.
Table 1: Definitions

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Literature search

A search was conducted using the Ovid MEDLINE database to explore axillary artery branching variations documented in the literature from 1946 to 2019. The Medical Subject Headings (MeSH) term “axillary artery” was used, and text words included axillary artery, branch pattern, and branch variation. The corresponding MeSH term and text words were combined using the Boolean operator “OR” then each set of terms were combined using the Boolean operator “AND”. Results were limited to humans and English language articles, resulting in 18 citations [Table 2]. Variations documented in the literature were summarized, with 31 branching variants noted among 948 total limbs. The prevalence of these variations was compared to the variations observed most frequently in this study. Bergman's Comprehensive Encyclopedia of Human Anatomic Variation [14] was also consulted for variants not captured by the literature search articles.
Table 2: Literature search results

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Statistical analysis

A Chi-square goodness of fit test with post hoc analyses on the adjusted standardized residuals was used to evaluate the branching patterns. The analyses assessed two research questions:

  1. Did the observed frequency of the classic presentation of the axillary artery [Figure 1] and [Table 1] in the cadaveric specimens differ significantly from the expected frequency of this arrangement? A Chi-square goodness of fit test was used to assess this question (alpha = 0.05)
  2. If the observed frequency is significantly different from the expected frequency, which variants contribute most to the significant Chi-square value? To assess this question the frequency of each branching pattern variant was recorded, and post hoc tests were run on the adjusted standardized residuals to determine the most significant variants.[15] The Bonferroni adjusted alpha for the post hoc analyses was 0.003125.


All statistical analyses were performed using SPSS software, version 26, IBM Corporation (SPSS Inc., USA).[16]


  Results Top


Variable and conserved branches of the axillary artery

The locations of the lateral thoracic and posterior circumflex humeral arteries were significantly variable [Table 3]. Variant presentations of these arteries were encountered significantly more frequently than the classic presentation in this study population. The lateral thoracic and posterior circumflex humeral arteries were only observed in their textbook locations in 40.3% and 61.3% of cases, respectively [Figure 2].
Table 3: Post hoc analysis of standardized adjusted residuals

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Figure 2: Frequency of the classic presentation of each axillary artery branch

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Post hoc analysis indicated that the LTA was the most variable axillary artery branch in our study population, assuming the classic presentation in fewer than half of the dissected limbs (40.3%) [Table 3]. It originated from the thoracodorsal artery in 37% of cases and from the SSA in 21% of cases [Figure 3]. The second most variable branch was the PCHA, assuming the classic presentation in 61.3% of the dissections [Figure 2]. The most common variant presentation involved the PCHA originating from the SSA in 19.4% of cases [Figure 4]. The second most frequently observed variant was a common trunk for the PCHA and ACHA arising from the axillary artery [13%; [Figure 4].
Figure 3: Most frequently observed variations of the lateral thoracic artery. Illustration credit: Austin Pena

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Figure 4: Representation of the posterior circumflex humeral artery arising from the subscapular artery and from a common trunk with the anterior circumflex humeral artery. Illustration credit: Austin Pena

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The locations of the superior thoracic, thoracoacromial, and subscapular arteries were significantly conserved and documented in their textbook branchpoint locations in 97%–98% of cases [Table 3]. The classic presentation of these branches was observed significantly more frequently than variations.

Literature search: Comparative frequencies

Classic branching distribution of the axillary artery

Studies in the literature search also report variants more frequently than the classic presentation. Astik and Dave [17] reported the normal pattern of distribution in 37.5% of limbs, whereas Huelke [18] reported 26.7%, Maheswary et al.[19] reported 20%, and Lippert and Pabst [20] observed only 10% of limbs with the classic branching pattern.

Lateral thoracic artery

The frequency of the classic presentation of the LTA in the literature search studies ranged from 40% to 78.3%.[18],[21],[22],[23],[24],[25],[26] Huelke [18] reported the LTA arising directly from the second part of the axillary artery in 52.2% of cases, with the next most common presentation being an origin from the thoracodorsal or SSA (28.7%). The LTA arose from the SSA in 8.6% of the 948 cases summarized in the literature search.[17],[18],[22],[27],[28],[29],[30] The literature also reported inconsistencies in variants, potentially a result of population variation or of how the variant is defined. For example, Poynter [31] reported that the LTA is doubled in 24% of individuals, whereas Olinger [32] reports this variant in only 6% of cases. The most inconsistently reported variant in the literature is the origin of the LTA from the thoracoacromial artery, a variant not observed in the current study. Frequencies of this presentation ranged between 0% and 73.2%, with a standard deviation of 25% among the studies.[18],[20],[21],[23],[24],[25],[26],[31],[33],[34],[35],[36],[37] Paraskevas [34] and Lee et al.[36] surmised that these discrepancies are likely due to the use of different criteria to define the LTA.

Posterior circumflex humeral artery

The classic presentation of the PCHA ranged from 33% to 77% in the literature search.[18],[21],[22],[23],[24],[25],[26] The PCHA was documented as originating from the SSA in 13% of the total cases in the literature search. The frequency of this variant among individual studies ranged from 1.4% to 39.8%.[18],[21],[22],[23],[24],[25],[26],[32],[38],[39],[40] A common trunk for PCHA and ACHA arising directly from the axillary artery was documented in 7% of total cases in the literature search; the frequency among individual studies ranged between 6% and 27.9%.[18],[21],[24],[25],[26],[31],[32],[37]

Superior thoracic, thoracoacromial, and subscapular arteries

These three branches were the most constant of the axillary branches with respect to the classic presentation, a finding consistent with other reports.[18],[21],[23],[24],[31],[41] The superior thoracic artery is the most consistent in its presentation.[32] Authors varied in terms of what they labeled as the SSA versus a “common trunk” for the SSA and any number of other branches, including the PCHA, ACHA, LTA, thoracodorsal, thoracoacromial, circumflex scapular, and profunda brachii arteries.[17],[27],[31],[32],[42],[43],[44],[45],[46],[47],[48],[49],[50] For example, Lengele and Dhem [51] named a “thoracodorso-subscapular trunk,” while Saeed et al.[46] referred to a “subscapular-circumflex humeral trunk” and Olinger [32] reports a common trunk for the SSA and the LTA about 10% of the time. Regardless, the SSA consistently gives rise to the circumflex scapular artery and the thoracodorsal artery.[40]


  Discussion Top


Collectively, the results of this statistical analysis and literature review indicate that the classic axillary artery branching pattern students expect to find in cadavers and patients rarely occurs. The classic presentation of the axillary artery branches was observed in <20% of this study sample. Other studies have documented a considerable variation in the axillary artery branching pattern, with the highest occurrence of the classic presentation reported in only 37.5% of individuals.[17],[18],[19],[20] Perhaps the persistence of teaching the classic pattern is because of the ease of memorizing that one branch arises from the first part of the artery, two branches arise from the second part, and three branches from the third part. However, this implies that the axillary artery possesses distinctive morphological characteristics,[2] when in reality, variation in the axillary artery branching pattern is the rule rather than the exception.[17] This presents an issue in clinical anatomy education because the morphology emphasized in anatomy courses does not reflect accurately what practitioners encounter in the patient population. This leads to the question: why teach the axillary artery branching pattern depicted frequently as the “normal” presentation, when it differs considerably from what medical learners likely will observe in their patients?

This study illustrates the need for re-evaluation of the “typical” position of major axillary artery branches, specifically the LTA and PCHA. The statistical analysis indicated that variations most often involve these branches, and these variants have received considerable attention in the literature.[17],[18],[19],[21],[22],[23],[24],[26],[31],[32],[33],[37],[38],[39],[52] The superior thoracic, thoracoacromial, and subscapular arteries often arise from the first, second and third parts of the axillary artery, respectively, as classically presented.[18],[21],[23],[24],[31],[41] Branches arising from the SSA may be variable and complex, but the SSA usually arises from the third part of the axillary artery and consistently gives rise to the circumflex scapular and thoracodorsal arteries.[18],[21],[22],[23],[24],[25],[26],[38],[39],[40]

Familiarity with common variations is important in interpreting radiological images, explaining unexpected clinical signs and symptoms, and informing surgical and interventional procedures.[17],[33] Axillary artery anatomy is clinically important for trauma reconstruction, administering local anesthesia to the brachial plexus, interventions for surgical neck fractures and subluxations of the humerus, axillary artery thrombosis, axillary-coronary bypass shunts, antegrade cerebral perfusion in aortic surgery, breast tumor resection and reconstruction, and various pedicles and flap reconstructions.[17],[22],[33],[36],[38],[47],[53],[54],[55],[56],[57] The highly variable LTA and PCHA are essential to many of these procedures. For example, the LTA supplies a significant portion of the breast and nipple-areolar complex and is therefore important in therapeutic, cosmetic, and reconstructive breast surgeries.[33],[58] The LTA is also used as a recipient vessel in a number of upper extremity free flap procedures.[22],[33],[55],[56],[59] The PCHA is important in treating surgical neck fractures and performing reconstructive flap procedures.[22],[54],[60],[61] Olinger and Benninger [22] report extensively on the clinical significance of PCHA variants. They found that when the PCHA arises from the axillary artery, SSA, and LTA, it always traverses the quadrangular space with the axillary nerve. However, when the PCHA originated from the profunda brachii, these landmarks for locating the vessel became unreliable, with 86% in the triangular interval and only 14% in the quadrangular space.

While cadaveric dissection is arguably the most effective means for medical students to develop an appreciation of anatomic variation and establish anatomical competence.[62],[63],[64],[65] Virtual anatomy platforms are being incorporated into curricula at an accelerated pace to accommodate social distancing and remote education solutions to the COVID-19 pandemic.[8] Educators must be cognizant of the capacity of these learning modalities to provide a representative experience of anatomic complexity. Similarly, education technology developers should be familiar with the most common anatomical variants and their clinical significance when developing content for medical learners. Digital resources documenting anatomical variations are accessible to learners (e.g., particularly via the web version of Bergman's Illustrated Encyclopedia of Human Anatomic Variation [66]), and educators can use these resources to develop relevant activities and assignments. Educators should emphasize common variants with clinical relevance to present a realistic picture of anatomic complexity and raise awareness about potential clinical implications of overlooking anatomical variations.

Study limitations

This research statistically assesses the educational relevance of the classic axillary artery branching pattern, but several study limitations should be considered. The sample size was relatively small, and the population came from the mid-Western United States and may not be representative of all populations. However, it should be noted that a number of the articles captured by the literature search included fewer donors, and some were case reports on a single individual. The literature search was not a formalized systematic review or meta-analysis. The majority of articles did not provide anatomical criteria for identifying and classifying axillary artery branches. This absence of precise descriptions of the anatomical area of distribution and/or landmarks may introduce interobserver variation in reported frequencies of anatomical variants, accounting for notable differences between studies.[34],[36] To address this in our study, we created a table with definitions and criteria for naming the axillary artery branches [Table 1].


  Conclusion Top


The results of this analysis and literature review indicate that axillary artery variation is the rule, rather than the exception. Over the course of 2 years of the MCASOM Arizona anatomy course, only 17.7% of upper limbs displayed the “textbook” presentation. The LTA and PCHA were most often observed in variant locations, while the superior thoracic, thoracoacromial, and subscapular arteries were most often found in their textbook locations. These results suggest the classic depiction of the axillary artery is not clinically relevant, as it does not reflect what students are likely to encounter in clinical practice. This is noteworthy because axillary artery branches are relevant in a number of surgical procedures. This study highlights a need to reevaluate what is defined as 'typical' regarding the major axillary artery branching morphology.

Acknowledgments

The authors would like to recognize Austin Pena, a 3rd-year medical student at MCASOM Arizona, for the creation of the anatomical illustrations used in this publication. We would also like to thank Dr. Scott Kriegshauser, MD, Mayo Clinic Arizona Department of Radiology, for confirming the anatomy on computed tomography scans of the cadavers, and Lisa Marks for her assistance with the literature search. We are grateful to the individuals who selflessly donate their bodies for medical science research and education; without them this study would not have been possible.

Ethics approval

The use of human cadavers in this study was approved by the Mayo Clinic Biospecimens Subcommittee (proposal number: 19000378).

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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