588129
research-article2015
AORXXX10.1177/0003489415588129Annals of Otology, Rhinology & LaryngologyScali et al
Original Article
Defining the Morphology and Distribution of the Alar Fascia: A Sheet Plastination Investigation
Annals of Otology, Rhinology & Laryngology 1–6 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0003489415588129 aor.sagepub.com
Frank Scali, DC1, Lance G. Nash, PhD2, and Matthew E. Pontell, MD3
Abstract Objectives: This study aims to delineate the morphology, integrity, and distribution of the alar fascia using dissection and E12 sheet plastination. This is the first study that employs E12 sheet plastination to investigate the alar fascia and its adjacent potential spaces. Methods: Twenty-nine manual dissections and 3 sets of E12 sheet plastinations were used to examine the posterior pharyngeal region for the architecture and distribution of the alar fascia. Specimens were examined from the inferior nuchal line to C6. Results: The alar fascia originated as a well-defined midline structure at the level of C1 and could be identified down to C6. There was no evidence of the alar fascia between the inferior nuchal line and the base of the skull. Notably, the alar fascia permitted resistance to manual traction. Conclusions: E12 sheet plastination allowed for visualization of the alar fascia’s superior attachments within the deep cervical region. Resistance to traction suggests that the alar fascia may be more than just a loose fibroareolar matrix. The findings in this study suggest an alternative point of entry into the danger space. Understanding the continuity of this fascial layer is critically important with regard to the pathophysiology of deep neck space infections. Keywords alar, plastination, retropharyngeal, prevertebral, fascia, mediastinitis
Introduction Since its first description in the early 20th century, the alar fascia has been included in numerous reports regarding the retropharyngeal and prevertebral spaces.1-9 Defined as a loose fibroareolar membrane within the retropharyngeal region, the alar fascia intervenes the potential space between visceral (buccopharyngeal) and prevertebral fasciae, extending distally between the first through sixth thoracic vertebrae. This tissue plane separates the retropharyngeal space (RS) into 2 potential spaces of clinical relevance: the true RS and prevertebral (danger) space (DS).10-16 Differing descriptions of the RS and DS exist in the clinical literature.16-18 The most common discordance is found within radiological studies, in which the alar fascia is ignored. Since invasive lesions within the DS or RS cannot be differentiated with modern imaging modalities, the 2 spaces are considered as one.2,19-27 Anatomically, the 3 layers of the deep cervical fascia and potential spaces have not been extensively evaluated since their classical descriptions in 1934.1 In fact, reports remain inconsistent concerning whether or not the alar fascia extends to the base of the skull.1,2,4,5,15,25,27-32 Limitations when describing the alar
fascia are mainly attributed to difficulties in dissecting fascial spaces by conventional measures. It is also widely stated that the ability to properly identify retropharyngeal spaces is limited by the looser fibroareolar structure of the alar fascia in comparison to its adjacent buccopharyngeal and prevertebral fasciae.10,25,27-29 This arrangement compromises proper separation of fascial layers during dissection.10,12 Considering restrictions regarding dissection and conventional imaging modalities, our understanding of the alar fascia (and adjacent spaces) continues to be defined by anatomic and clinical descriptions from the early 20th century. 1
American University of the Caribbean School of Medicine, Cupecoy, St. Maarten 2 Department of Anatomy, American University of the Caribbean School of Medicine, Cupecoy, St Maarten 3 Department of Surgery, Drexel University College of Medicine, Philadelphia, PA, USA Corresponding Author: Frank Scali, American University of the Caribbean School of Medicine, 1411 Balsam Willow Trail, Orlando, FL 32825, USA. Email: [email protected]
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Comprehensive description of the alar fascia is essential in order to understand the etiology, complications, and direction of the spread of disease in the neck.18 It also serves as an anatomical guide for retropharyngeal lymphadenectomy.10 This study aims to define and clarify the morphology and distribution of the upper fibers of the alar fascia between the first (C1) and sixth (C6) cervical vertebrae and to investigate alternate entry points into the DS. E12 sheet plastination provides an original approach in the analysis and interpretation of the anatomical arrangement that composes the alar fascia.
Materials and Methods Thirty-two cadavers (17 male, 15 female; 67 to 89 years) were examined in this study. Specimens showed no signs of prior surgery, trauma, or variations in the area of interest. Three specimens (2 male, 1 female) preserved using the E12 sheet plastination procedure were selected from the Department of Anatomy at the American University of the Caribbean, School of Medicine. Twenty-nine specimens underwent gross dissection, which were obtained from the Department of Anatomy and Structural Biology at Otago University, School of Medical Sciences. This study was conducted in accordance with all protocols for cadaveric research. Three cadavers were prepared as sets of 2-mm thick epoxy resin slices using E12 sheet plastination technique.33 Preparation required embalming of cadaveric specimens followed by freezing at −85°C for 48 hours. Once frozen, each specimen was sectioned, then dehydrated and degreased by immersing tissue slices into acetone chilled at −25°C. Acetone concentration was gradually increased over a period of 20 to 22 weeks until the dehydration and degreasing process was approved based on tissue clarity, shrinkage, and preservation. The next step was vacuum impregnation of resin mixture conducted under cryogenic conditions (−8°C to 0°C) over a 2-day period. Impregnation was complete when bubbles failed to appear from tissue specimens. Sections were then laminated by being placed in a warm water bath followed by an oven set at 35°C for 24 hours to achieve solidification. Translucent plastinations were initially examined on a radiographic light box. Each slice was subsequently reviewed macroscopically under low magnification (range 0.63× to 1.25×) under a Leica MZ8 Stereoscopic Dissecting Microscope. Fibrous architecture and distribution of the alar fascia was observed in the posterior pharyngeal region between the pretracheal and prevertebral layers. Transverse slices were examined at variable levels of the suprahyoid and infrahyoid neck to identify continuity of the alar fascia. Photographs were captured with a Nikon Coolpix 900 Digital Camera.
Twenty-nine specimens (15 male, 14 female) underwent wedge osteotomy resection of the posterior cranial fossa in order to access the RS. Soft tissue overlying the calveria was removed in order to prepare for a craniotomy. A circumferential continuous cut was performed approximately 1.5 cm above the occipital protuberance, external auditory meatus, and superciliary ridge of each cadaver using an oscillating Stryker Autopsy 810 electric saw. Coronal cuts were made at the midline of the clivus with an oscillating saw approximately 2 cm anterior to the foramen magnum. The occipital bone, along with the posterior cranial fossa, was reflected posteriorly exposing the RS to the level of the fourth cervical vertebra (C4). Structures of interest were identified and photographed.
Results Similar observational patterns were identified in all cadavers at distinct vertebral levels within the plastinated transverse sections. At the level of the inferior nuchal line, the alar fascia was absent. Instead, the area between the posterior pharyngeal wall and the longus capitis contained loose fibroareolar connective tissue. The buccopharyngeal and prevertebral fasciae appeared as an arrangement of disordered fibrous bands, which traversed posteriorly along the midsaggital plane between the right and left longus capitis muscles (Figure 1a). Between the occiput and C1, a midline fibrous layer signified the beginning of the alar fascia. The buccopharyngeal fascia was difficult to identify due to haphazard arrangement of its fibers. In contrast, the prevertebral fascia was clearly a delineation of epimysium covering the anterior surface of the longus cervicus and longus colli (Figure 1b). At the conjunction of C1 and the second (C2) cervical vertebrae, the buccopharyngeal and prevertebral fasciae were easily recognized and well demarcated. The alar fascia was identified as a continuous membrane spanning the space between these 2 layers. Laterally, the alar fascia extended fibers to the medial aspect of the carotid sheaths surrounding the internal and external carotid arteries (Figure 2c). At the level of C4, the alar fascia remained as a distinct membrane located between the buccopharyngeal and prevertebral layers. The alar fascia appeared to arise from the medial wall of the carotid sheath and from the medial raphe extensions from the posterior middle pharyngeal constrictor (Figure 2d). The alar fascia was clearly identified in the infrahyoid region (C6). The morphology of the alar fascia was similar to that observed in the suprahyoid region, except the carotid sheath invested the common carotid artery (Figure 3e).
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Figure 1. (a) Magnified plastinated transverse section at the level of the inferior nuchal line (see line “a” depicted on illustration). The space between the posterior muscular wall of the pharynx and the longus capitis (LCa) consists of loose fibrous tissue with no evidence of an alar fascia (triple asterisks). The carotid vessels are isolated medially by the levator veli palatini (LVP), and part of its medial wall is formed by the fascia (black arrows) of rectus capitis anterior (RCA). Also labeled: temporal bone (TMP), lateral pterygoid muscle (LPG), internal carotid artery (ICA), external carotid artery (ECA), occipital bone (OC), anterior longitudinal ligament (ALL), and tensor veli palatine (TVP). Scale bar = 5 mm. (b) Magnified plastinated transverse section at the level between the foramen magnum and C1 (see line “b” depicted on illustration). At the occipital level, the buccopharyngeal fascia was difficult to identify due to the haphazard orientation of its fibers. The prevertebral fascia (black arrows) was formed from the longus capitis (LCa) fascia and was in close proximity to the medial aspect of the superior pharyngeal constrictor (SPC) wall. A midline fibrous layer signified the beginning of the alar fasica (white arrowhead). Also labeled: fibroareolar space between the epimysium of the levator veli palatine and buccopharyngeal fascia (triple asterisks), levator veli palatine (LVP), anterior longitudinal ligament (ALL), internal carotid artery (ICA), longus colli (LCo), medial pterygoid (MPG), stylopharyngeus (STP), C1 vertebra (C1), and parapharyngeal fat pad (PPFP). Scale bar = 5 mm.
Gross dissection revealed a network of disordered soft tissue tracts above the level of C1, none of which could be identified as a specific or single layer of fascia. A thickened midline conjunctive tract beginning 2 cm below the apex of the odontoid process, immediately superior to the anterior tubercle of the atlas, signified the origin of the alar fascia. The alar fascia diverged laterally and separated into a loose fibroareolar matrix anteriorly as the posterior cranial fossae was hinged posteriorly. The underlining membrane maintained its integrity when traction was applied in all planes using toothed forceps. As anterior traction was applied, evidence of a separate layer posterior to the alar fascia was identified as the prevertebral fascia (Figure 3f).
Discussion This investigation delineates the origin and anatomical morphology of the alar fascia in the cervical region
using E12 sheet plastination. Aside from supplementing existing information regarding the alar fascia, E12 sheet plastination has provided additional evidence regarding the origin of the alar fascia as well as the in situ organization of the potential spaces occupying the retropharyngeal region. Classical and contemporary reports remain inconsistent concerning extension of the alar fascia to the base of the skull.1,2,4,5,15,25,27-29,32 Results of this study reveal that the alar fascia begins at the level of C1 whereas loose fibroareolar connective tissue occupies the space between the inferior nuchal line and base of the skull. This transitional level may indicate an alternative point of infectious breach into the DS. Gross dissection revealed the alar fascia was comparable in thickness and integrity to the buccopharyngeal and prevertebral fasciae (Figure 4). This finding is inconsistent with reports regarding the alar fascia as a simple loose layer offering relatively poor resistance to infectious spread.15,34 Identified as a dense structure, the
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Figure 2. (c) Magnified plastinated transverse section at C2 vertebral level (see line “c” depicted on illustration). The prevertebral fascia (black arrows) and buccopharyngeal fascia (white arrowheads) were found to be well established. Between these 2 fascial layers, the alar fascia (white arrows) spans the intervening space. The alar fascia divides the potential space to form the retropharyngeal space (single asterisk) and the danger space (double asterisk). Also labeled: external carotid artery (ECA), middle pharyngeal constrictors (MPC), longus colli (LCo), longus capitis (LCa), and the body of the second cervical vertebra (C2). Scale bar = 2.5 mm. (d) Magnified plastinated transverse section at the level of the hyoid bone (see line “d” depicted on illustration). Image reveals the alar fascia (white arrows) between the pretracheal layer (white arrowheads) anteriorly and prevertebral layer (black arrows) posteriorly. The fibrous arrangement of the alar fascia appeared to arise from the medial wall of the carotid sheath and from medial raphe extensions of the posterior middle pharyngeal constrictor (MCP). The alar fascia fused to 2 flanking fasciae at the middle (triple asterisks). Also labeled: hyoid bone (HYD), longus capitis (LCa), and the body of the fourth cervical vertebra (C4). Scale bar = 2.5 mm.
alar fascia may influence direction of spread of diseases in the neck. Various radiological studies indicate the alar fascia lacks characteristics of a distinct fibrous structure, and therefore is not considered its own layer.15,27-29,34 Results of this study contradict these reports. Inability to differentiate the alar fascia as a separate layer implies that it is frequently overlooked.22-24,26 If the alar fascia is ignored, there is a misinterpretation in the number of potential spaces present, which may affect clinical management of deep neck space infections.22 The alar fascia is, however, occasionally identified with contrast-enhanced computerized tomography in edematous patients with post–radiation therapy.3 It is also commonly reported that the alar and prevertebral fasciae contribute to the posterior aspect of the carotid sheath.15,34,35 The results indicate that the lateral fibers of the alar fascia contributed largely to the medial aspect of the carotid sheath. This may be of clinical relevance considering spread of infection into the carotid space (Lincoln’s Tunnel) poses a threat to the vital structures located within this space.22
A limitation of E12 sheet plastination technique is that the process may shrink soft tissue structures such as muscle. However, this process permits separation of fascial planes and a clearer delineation of the DS, which otherwise is difficult to dissect by conventional methods. Therefore, this “limitation” inadvertently provides a credible method for identifying the alar facial layer and its adjacent spaces in situ. Defined for centuries using conventional dissection techniques, this is the first study that employs E12 sheet plastination in the investigation of the alar fascia in situ and its association with adjacent potential spaces. Appropriate management of deep neck infections is highly reliant on diagnostic imaging when determining the location and extent of involvement.36,37 As a structural component of both the RS and DS, the alar fascia should not be overlooked as a potential barrier when discussing spaces of origin or routes of infection in anatomically based differential diagnoses. This study may also assist in preoperative planning of retropharyngeal lymphadenectomy.10,15
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Figure 3. (e) Magnified plastinated transverse section in the infrahyoid neck at the C6 vertebral level (see line “e” depicted on illustration). The alar fascia (white arrows) traverses the space between the pretracheal layer (white arrowheads) and the prevertebral layer (black arrowheads) and forms part of the medial wall of the carotid sheath. What appears to be the alar and prevertebral fascia fusing along part of their length indicates overlapping artifact of the 2 membranes during the sheet plastination procedure. Also labeled: retropharyngeal space (single asterisk), danger space (double asterisks), external carotid artery (†), longus colli (LCo), and the body of the sixth cervical vertebra (C6). Scale bar = 2.5 mm. (f) Image depicts a superior to inferior view of the retropharyngeal space following a wedge osteotomy resection of the posterior cranial fossa (see line “f” depicted on illustration). Anterior traction is being placed on the alar fascia (a) revealing its integrity and the potential space between it and the prevertebral fascia (b). Also labeled: apex of the odontoid process (single asterisk) and the loose fibroareolar consistency (double asterisks) of the retropharyngeal space due to separation of the alar fascia from the buccopharyngeal fascia following wedge osteotomy.
Acknowledgments The authors would like to thank Dr Ming Zhang, MD, PhD and Professor Helen Nicholson, MD for their generous contribution and assistance in making this study possible. The authors would also like to thank Rachel Lilyquist, RN for proofreading this article. Original anatomical illustration created by Frank Scali, DC.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References Figure 4. Image depicts a transverse cut of the cervical spine revealing 3 distinct and separate layers of fascia located within the retropharyngeal space. The buccopharyngeal fascia (white arrowheads) and alar fascia (asterisks) form the potential space identified as the retropharyngeal space (RS). The alar and prevertebral fasciae (black arrows) form the potential space identified as the danger space (DS). Each layer appears similar in thickness and consistency as traction was applied. Note the loose connective tissue between each fascial layer. Also labeled: esophagus (Oe) and trachea (Tr).
1. Grodinsky M, Holyoke EA. The fasciae and fascial spaces of the head, neck and adjacent regions. Am J Anat. 1934;63: 367-407. 2. Levitt GW. Cervical fascia and deep neck infections. Laryngoscope. 1970;80:409-435. 3. Mukherji SK, Castillo M. A simplified approach to the spaces of the suprahyoid neck. Radiol Clin North Am. 1998;36:761-780. 4. Granich MS, Klotz RE, Lofgren RH, Partlow RC, DiGregorio LI. Spontaneous retropharyngeal and cervical subcutaneous emphysema in adults. Arch Otolaryngol. 1983;109:701-704.
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5. Scott BA, Stiernberg CM, Driscoll BP. Deep neck space infections. In: Bailey BJ, ed. Head and Neck Surgery Otolaryngology. Philadelphia, PA: Lippincott-Raven; 1998:819-835. 6. Rouviere H. Lymphatic System of the Head and Neck. Anatomy of Human Lymphatic System. Ann Arbor, MI: Edwards Rothers; 1938. 7. Burns A. Observations of the surgical anatomy of the head and neck. In: Charpy A, ed. Aponeuroses de Cou: Traite d’Anatomie Humain. Paris, France: Maisson et Cie; 1912. 8. Charypy A. Aponeuroses de Cou: Traite d’Anatomie Humain. Paris, France: Maisson et Cie; 1912. 9. Dean LW. The proper procedure for external drainage of retropharyngeal abscesses secondary to caries of the vertebrae. Ann Otol Rhinol Laryngol. 1919;28:566. 10. Ozlugedik S, Acar HI, Apaydin N, et al. Retropharyngeal space and lymph nodes: an anatomical guide for surgical dissection. Acta Otolaryngol. 2005;125:1111-1115. 11. Owens DE, Calcaterra TC, Aarstad RA. Retropharyngeal hematoma: a complication of therapy with anticoagulants. Arch Otolaryngol. 1975;101:565-568. 12. Davis WL, Harnsberger HR, Smoker WR, Watanabe AS. Retropharyngeal space: evaluation of normal anatomy and diseases with CT and MR imaging. Radiology. 1990;174:59-64. 13. Chong VF, Fan YF. Radiology of the retropharyngeal space. Clin Radiol. 2000;55:740-748. 14. Perrott JW. Anatomical aspects of hypopharyngeal diverticula. Aust N Z J Surg. 1961;31:307-317. 15. Vieira F, Allen SM, Stocks RMS, Thompson JW. Deep neck infection. Otolaryngol Clin North Am. 2008;41:459-483. 16. Debnam JM, Guha-Thakurta NG. Retropharyngeal and prevertebral spaces: anatomic imaging and diagnosis. Otolaryngol Clin North Am. 2012;45:1293-1310. 17. Standring S. Gray’s Anatomy: The Anatomical Basis of Clinical Practice. 40th ed. Philadelphia, PA: Elsevier Saunders; 2008:438-439. 18. Levitt GW. Cervical fascia and deep neck infections. Otolaryngol Clin North Am. 1976;9:703-716. 19. Cross RR, Shapiro MD, Som PM. MRI of the parapharyngeal space. Radiol Clin North Am. 1989;27:353-378. 20. Davis WL, Smoker WR, Harnsberger HR. The normal and diseased retropharyngeal and prevertebral spaces. Semin Ultrasound CT MR. 1990;11:520-533. 21. Gianoli M, Espinola TE, Guarisco JL, Miller RH. Retropharyngeal space infection: changing trends. Otolaryngol Head Neck Surg. 1991;105:92-100. 22. Graney DO, Sie KCY. Developmental anatomy. In: Cummings CW, Friedrickson JM, Harker LA, Krause CJK,
Schuller DE, eds. Pediatric Otolaryngology Head and Neck. 3rd ed. St Louis, MO: Mosby; 1992. 23. Weber AL, Baker AS, Montgomery WW. Inflammatory lesions of the neck, including fascial spaces—evaluation by computed tomography and magnetic resonance imaging. Isr J Med Sci. 1992;28:241-249. 24. Carlson GW. Surgical anatomy of the neck. Surg Clin North Am. 1993;73:837-852. 25. Williams DW. An imager’s guide to normal neck anatomy. Semin Ultrasound CT MR. 1997;18:157-181. 26. Lingeman RE. Surgical anatomy. In: Cummings CW, Fredrickson JM, Krause LA, Harker TH, Schuller DE, Richardson MA, eds. Otolaryngology Head and Neck Surgery. Vol. 3. St Louis, MO: Mosby-Year Book; 1998. 27. Wippold FJ. Neck. In: Lee JKT, Stanley RJ, Heiken JP, eds. Computed Body Tomography With MRI Correlation. Vol. 1. Philadelphia, PA: Lippincott-Raven; 1998:107-182. 28. Harnsberger HR. Handbook of Head and Neck Imaging. 2nd ed. St Louis, MO: Mosby Year-Book; 1995. 29. Williams DW. Neck imaging. In: Shockley WW, Pilsbury HC, eds. The Neck: Diagnosis and Surgery. St Louis, MO: Mosby; 1994:199-266. 30. Casberg MA. The clinic significance of the cervical fascial planes. Surg Clin North Am. 1950;30:1415-1435. 31. Grodinsky M. Retropharyngeal and lateral pharyngeal abscesses: an anatomic and clinical study. Ann Surg. 1939;110:177-199. 32. Shanker L, Cheung G, Khan A. Anatomy and spaces of the neck. In: Shanker L, Cheung G, Khan A, eds. Head and Neck Imaging. New York, NY: McGraw-Hill; 1998:1-14. 33. von Hagens G. Impregnation of soft biological specimens with thermosetting resins and elastomers. Anat Rec. 1979;194: 247-255. 34. Weed HG, Forest LA. Deep neck infection. In: Cummings CW, Flint PW, Harker LA, et al, eds. Otolaryngology: Head and Neck Surgery. Vol. 3. 4th ed. Philadelphia, PA: Elsevier Mosby; 2005:2515-2524. 35. Yellon RF. Head and neck space infections. In: Bluestone CD, Casselbrant ML, Stool SE, et al, eds. Pediatric Otolaryngology. Vol. 2. 4th ed. Philadelphia, PA: Saunders; 2003:1681-1701. 36. Nagy M, Backstrom J. Comparison of the sensitivity of lateral neck radiographs and computerized tomography scanning in pediatric deep-neck infections. Laryngoscope. 1999;109: 775-779. 37. Boscolo-Rizzo P, Marchiori C, Zanetti F, Vaglia A, Da Mosto MC. Conservative management of deep neck abscesses in adults: the importance of CECT findings. Otolaryngol Head Neck Surg. 2006;135:894-899.
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research-article2015
AORXXX10.1177/0003489415588129Annals of Otology, Rhinology & LaryngologyScali et al
Original Article
Defining the Morphology and Distribution of the Alar Fascia: A Sheet Plastination Investigation
Annals of Otology, Rhinology & Laryngology 1–6 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0003489415588129 aor.sagepub.com
Frank Scali, DC1, Lance G. Nash, PhD2, and Matthew E. Pontell, MD3
Abstract Objectives: This study aims to delineate the morphology, integrity, and distribution of the alar fascia using dissection and E12 sheet plastination. This is the first study that employs E12 sheet plastination to investigate the alar fascia and its adjacent potential spaces. Methods: Twenty-nine manual dissections and 3 sets of E12 sheet plastinations were used to examine the posterior pharyngeal region for the architecture and distribution of the alar fascia. Specimens were examined from the inferior nuchal line to C6. Results: The alar fascia originated as a well-defined midline structure at the level of C1 and could be identified down to C6. There was no evidence of the alar fascia between the inferior nuchal line and the base of the skull. Notably, the alar fascia permitted resistance to manual traction. Conclusions: E12 sheet plastination allowed for visualization of the alar fascia’s superior attachments within the deep cervical region. Resistance to traction suggests that the alar fascia may be more than just a loose fibroareolar matrix. The findings in this study suggest an alternative point of entry into the danger space. Understanding the continuity of this fascial layer is critically important with regard to the pathophysiology of deep neck space infections. Keywords alar, plastination, retropharyngeal, prevertebral, fascia, mediastinitis
Introduction Since its first description in the early 20th century, the alar fascia has been included in numerous reports regarding the retropharyngeal and prevertebral spaces.1-9 Defined as a loose fibroareolar membrane within the retropharyngeal region, the alar fascia intervenes the potential space between visceral (buccopharyngeal) and prevertebral fasciae, extending distally between the first through sixth thoracic vertebrae. This tissue plane separates the retropharyngeal space (RS) into 2 potential spaces of clinical relevance: the true RS and prevertebral (danger) space (DS).10-16 Differing descriptions of the RS and DS exist in the clinical literature.16-18 The most common discordance is found within radiological studies, in which the alar fascia is ignored. Since invasive lesions within the DS or RS cannot be differentiated with modern imaging modalities, the 2 spaces are considered as one.2,19-27 Anatomically, the 3 layers of the deep cervical fascia and potential spaces have not been extensively evaluated since their classical descriptions in 1934.1 In fact, reports remain inconsistent concerning whether or not the alar fascia extends to the base of the skull.1,2,4,5,15,25,27-32 Limitations when describing the alar
fascia are mainly attributed to difficulties in dissecting fascial spaces by conventional measures. It is also widely stated that the ability to properly identify retropharyngeal spaces is limited by the looser fibroareolar structure of the alar fascia in comparison to its adjacent buccopharyngeal and prevertebral fasciae.10,25,27-29 This arrangement compromises proper separation of fascial layers during dissection.10,12 Considering restrictions regarding dissection and conventional imaging modalities, our understanding of the alar fascia (and adjacent spaces) continues to be defined by anatomic and clinical descriptions from the early 20th century. 1
American University of the Caribbean School of Medicine, Cupecoy, St. Maarten 2 Department of Anatomy, American University of the Caribbean School of Medicine, Cupecoy, St Maarten 3 Department of Surgery, Drexel University College of Medicine, Philadelphia, PA, USA Corresponding Author: Frank Scali, American University of the Caribbean School of Medicine, 1411 Balsam Willow Trail, Orlando, FL 32825, USA. Email: [email protected]
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Comprehensive description of the alar fascia is essential in order to understand the etiology, complications, and direction of the spread of disease in the neck.18 It also serves as an anatomical guide for retropharyngeal lymphadenectomy.10 This study aims to define and clarify the morphology and distribution of the upper fibers of the alar fascia between the first (C1) and sixth (C6) cervical vertebrae and to investigate alternate entry points into the DS. E12 sheet plastination provides an original approach in the analysis and interpretation of the anatomical arrangement that composes the alar fascia.
Materials and Methods Thirty-two cadavers (17 male, 15 female; 67 to 89 years) were examined in this study. Specimens showed no signs of prior surgery, trauma, or variations in the area of interest. Three specimens (2 male, 1 female) preserved using the E12 sheet plastination procedure were selected from the Department of Anatomy at the American University of the Caribbean, School of Medicine. Twenty-nine specimens underwent gross dissection, which were obtained from the Department of Anatomy and Structural Biology at Otago University, School of Medical Sciences. This study was conducted in accordance with all protocols for cadaveric research. Three cadavers were prepared as sets of 2-mm thick epoxy resin slices using E12 sheet plastination technique.33 Preparation required embalming of cadaveric specimens followed by freezing at −85°C for 48 hours. Once frozen, each specimen was sectioned, then dehydrated and degreased by immersing tissue slices into acetone chilled at −25°C. Acetone concentration was gradually increased over a period of 20 to 22 weeks until the dehydration and degreasing process was approved based on tissue clarity, shrinkage, and preservation. The next step was vacuum impregnation of resin mixture conducted under cryogenic conditions (−8°C to 0°C) over a 2-day period. Impregnation was complete when bubbles failed to appear from tissue specimens. Sections were then laminated by being placed in a warm water bath followed by an oven set at 35°C for 24 hours to achieve solidification. Translucent plastinations were initially examined on a radiographic light box. Each slice was subsequently reviewed macroscopically under low magnification (range 0.63× to 1.25×) under a Leica MZ8 Stereoscopic Dissecting Microscope. Fibrous architecture and distribution of the alar fascia was observed in the posterior pharyngeal region between the pretracheal and prevertebral layers. Transverse slices were examined at variable levels of the suprahyoid and infrahyoid neck to identify continuity of the alar fascia. Photographs were captured with a Nikon Coolpix 900 Digital Camera.
Twenty-nine specimens (15 male, 14 female) underwent wedge osteotomy resection of the posterior cranial fossa in order to access the RS. Soft tissue overlying the calveria was removed in order to prepare for a craniotomy. A circumferential continuous cut was performed approximately 1.5 cm above the occipital protuberance, external auditory meatus, and superciliary ridge of each cadaver using an oscillating Stryker Autopsy 810 electric saw. Coronal cuts were made at the midline of the clivus with an oscillating saw approximately 2 cm anterior to the foramen magnum. The occipital bone, along with the posterior cranial fossa, was reflected posteriorly exposing the RS to the level of the fourth cervical vertebra (C4). Structures of interest were identified and photographed.
Results Similar observational patterns were identified in all cadavers at distinct vertebral levels within the plastinated transverse sections. At the level of the inferior nuchal line, the alar fascia was absent. Instead, the area between the posterior pharyngeal wall and the longus capitis contained loose fibroareolar connective tissue. The buccopharyngeal and prevertebral fasciae appeared as an arrangement of disordered fibrous bands, which traversed posteriorly along the midsaggital plane between the right and left longus capitis muscles (Figure 1a). Between the occiput and C1, a midline fibrous layer signified the beginning of the alar fascia. The buccopharyngeal fascia was difficult to identify due to haphazard arrangement of its fibers. In contrast, the prevertebral fascia was clearly a delineation of epimysium covering the anterior surface of the longus cervicus and longus colli (Figure 1b). At the conjunction of C1 and the second (C2) cervical vertebrae, the buccopharyngeal and prevertebral fasciae were easily recognized and well demarcated. The alar fascia was identified as a continuous membrane spanning the space between these 2 layers. Laterally, the alar fascia extended fibers to the medial aspect of the carotid sheaths surrounding the internal and external carotid arteries (Figure 2c). At the level of C4, the alar fascia remained as a distinct membrane located between the buccopharyngeal and prevertebral layers. The alar fascia appeared to arise from the medial wall of the carotid sheath and from the medial raphe extensions from the posterior middle pharyngeal constrictor (Figure 2d). The alar fascia was clearly identified in the infrahyoid region (C6). The morphology of the alar fascia was similar to that observed in the suprahyoid region, except the carotid sheath invested the common carotid artery (Figure 3e).
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Figure 1. (a) Magnified plastinated transverse section at the level of the inferior nuchal line (see line “a” depicted on illustration). The space between the posterior muscular wall of the pharynx and the longus capitis (LCa) consists of loose fibrous tissue with no evidence of an alar fascia (triple asterisks). The carotid vessels are isolated medially by the levator veli palatini (LVP), and part of its medial wall is formed by the fascia (black arrows) of rectus capitis anterior (RCA). Also labeled: temporal bone (TMP), lateral pterygoid muscle (LPG), internal carotid artery (ICA), external carotid artery (ECA), occipital bone (OC), anterior longitudinal ligament (ALL), and tensor veli palatine (TVP). Scale bar = 5 mm. (b) Magnified plastinated transverse section at the level between the foramen magnum and C1 (see line “b” depicted on illustration). At the occipital level, the buccopharyngeal fascia was difficult to identify due to the haphazard orientation of its fibers. The prevertebral fascia (black arrows) was formed from the longus capitis (LCa) fascia and was in close proximity to the medial aspect of the superior pharyngeal constrictor (SPC) wall. A midline fibrous layer signified the beginning of the alar fasica (white arrowhead). Also labeled: fibroareolar space between the epimysium of the levator veli palatine and buccopharyngeal fascia (triple asterisks), levator veli palatine (LVP), anterior longitudinal ligament (ALL), internal carotid artery (ICA), longus colli (LCo), medial pterygoid (MPG), stylopharyngeus (STP), C1 vertebra (C1), and parapharyngeal fat pad (PPFP). Scale bar = 5 mm.
Gross dissection revealed a network of disordered soft tissue tracts above the level of C1, none of which could be identified as a specific or single layer of fascia. A thickened midline conjunctive tract beginning 2 cm below the apex of the odontoid process, immediately superior to the anterior tubercle of the atlas, signified the origin of the alar fascia. The alar fascia diverged laterally and separated into a loose fibroareolar matrix anteriorly as the posterior cranial fossae was hinged posteriorly. The underlining membrane maintained its integrity when traction was applied in all planes using toothed forceps. As anterior traction was applied, evidence of a separate layer posterior to the alar fascia was identified as the prevertebral fascia (Figure 3f).
Discussion This investigation delineates the origin and anatomical morphology of the alar fascia in the cervical region
using E12 sheet plastination. Aside from supplementing existing information regarding the alar fascia, E12 sheet plastination has provided additional evidence regarding the origin of the alar fascia as well as the in situ organization of the potential spaces occupying the retropharyngeal region. Classical and contemporary reports remain inconsistent concerning extension of the alar fascia to the base of the skull.1,2,4,5,15,25,27-29,32 Results of this study reveal that the alar fascia begins at the level of C1 whereas loose fibroareolar connective tissue occupies the space between the inferior nuchal line and base of the skull. This transitional level may indicate an alternative point of infectious breach into the DS. Gross dissection revealed the alar fascia was comparable in thickness and integrity to the buccopharyngeal and prevertebral fasciae (Figure 4). This finding is inconsistent with reports regarding the alar fascia as a simple loose layer offering relatively poor resistance to infectious spread.15,34 Identified as a dense structure, the
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Figure 2. (c) Magnified plastinated transverse section at C2 vertebral level (see line “c” depicted on illustration). The prevertebral fascia (black arrows) and buccopharyngeal fascia (white arrowheads) were found to be well established. Between these 2 fascial layers, the alar fascia (white arrows) spans the intervening space. The alar fascia divides the potential space to form the retropharyngeal space (single asterisk) and the danger space (double asterisk). Also labeled: external carotid artery (ECA), middle pharyngeal constrictors (MPC), longus colli (LCo), longus capitis (LCa), and the body of the second cervical vertebra (C2). Scale bar = 2.5 mm. (d) Magnified plastinated transverse section at the level of the hyoid bone (see line “d” depicted on illustration). Image reveals the alar fascia (white arrows) between the pretracheal layer (white arrowheads) anteriorly and prevertebral layer (black arrows) posteriorly. The fibrous arrangement of the alar fascia appeared to arise from the medial wall of the carotid sheath and from medial raphe extensions of the posterior middle pharyngeal constrictor (MCP). The alar fascia fused to 2 flanking fasciae at the middle (triple asterisks). Also labeled: hyoid bone (HYD), longus capitis (LCa), and the body of the fourth cervical vertebra (C4). Scale bar = 2.5 mm.
alar fascia may influence direction of spread of diseases in the neck. Various radiological studies indicate the alar fascia lacks characteristics of a distinct fibrous structure, and therefore is not considered its own layer.15,27-29,34 Results of this study contradict these reports. Inability to differentiate the alar fascia as a separate layer implies that it is frequently overlooked.22-24,26 If the alar fascia is ignored, there is a misinterpretation in the number of potential spaces present, which may affect clinical management of deep neck space infections.22 The alar fascia is, however, occasionally identified with contrast-enhanced computerized tomography in edematous patients with post–radiation therapy.3 It is also commonly reported that the alar and prevertebral fasciae contribute to the posterior aspect of the carotid sheath.15,34,35 The results indicate that the lateral fibers of the alar fascia contributed largely to the medial aspect of the carotid sheath. This may be of clinical relevance considering spread of infection into the carotid space (Lincoln’s Tunnel) poses a threat to the vital structures located within this space.22
A limitation of E12 sheet plastination technique is that the process may shrink soft tissue structures such as muscle. However, this process permits separation of fascial planes and a clearer delineation of the DS, which otherwise is difficult to dissect by conventional methods. Therefore, this “limitation” inadvertently provides a credible method for identifying the alar facial layer and its adjacent spaces in situ. Defined for centuries using conventional dissection techniques, this is the first study that employs E12 sheet plastination in the investigation of the alar fascia in situ and its association with adjacent potential spaces. Appropriate management of deep neck infections is highly reliant on diagnostic imaging when determining the location and extent of involvement.36,37 As a structural component of both the RS and DS, the alar fascia should not be overlooked as a potential barrier when discussing spaces of origin or routes of infection in anatomically based differential diagnoses. This study may also assist in preoperative planning of retropharyngeal lymphadenectomy.10,15
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Figure 3. (e) Magnified plastinated transverse section in the infrahyoid neck at the C6 vertebral level (see line “e” depicted on illustration). The alar fascia (white arrows) traverses the space between the pretracheal layer (white arrowheads) and the prevertebral layer (black arrowheads) and forms part of the medial wall of the carotid sheath. What appears to be the alar and prevertebral fascia fusing along part of their length indicates overlapping artifact of the 2 membranes during the sheet plastination procedure. Also labeled: retropharyngeal space (single asterisk), danger space (double asterisks), external carotid artery (†), longus colli (LCo), and the body of the sixth cervical vertebra (C6). Scale bar = 2.5 mm. (f) Image depicts a superior to inferior view of the retropharyngeal space following a wedge osteotomy resection of the posterior cranial fossa (see line “f” depicted on illustration). Anterior traction is being placed on the alar fascia (a) revealing its integrity and the potential space between it and the prevertebral fascia (b). Also labeled: apex of the odontoid process (single asterisk) and the loose fibroareolar consistency (double asterisks) of the retropharyngeal space due to separation of the alar fascia from the buccopharyngeal fascia following wedge osteotomy.
Acknowledgments The authors would like to thank Dr Ming Zhang, MD, PhD and Professor Helen Nicholson, MD for their generous contribution and assistance in making this study possible. The authors would also like to thank Rachel Lilyquist, RN for proofreading this article. Original anatomical illustration created by Frank Scali, DC.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
References Figure 4. Image depicts a transverse cut of the cervical spine revealing 3 distinct and separate layers of fascia located within the retropharyngeal space. The buccopharyngeal fascia (white arrowheads) and alar fascia (asterisks) form the potential space identified as the retropharyngeal space (RS). The alar and prevertebral fasciae (black arrows) form the potential space identified as the danger space (DS). Each layer appears similar in thickness and consistency as traction was applied. Note the loose connective tissue between each fascial layer. Also labeled: esophagus (Oe) and trachea (Tr).
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