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A review of the anatomy of soft tissues associated with sexually dimorphic landmarks on the cranium

Year 2022, Volume: 16 Issue: 2, 93 - 107, 30.08.2022

Abstract

Objectives: This review systematically assesses literature relating to five muscles and one ligament connected to sexually dimorphic cranial landmarks – the nuchal crest and mastoid process – used for sex estimation in anthropology: the upper trapezius, semispinalis capitis, sternocleidomastoid, splenius capitis, and longissimus capitis muscles and the nuchal ligament. Although these soft tissues are not commonly grouped together in anatomical literature, they are anthropologically relevant in relation to cranial sex estimation. This review demonstrates how anatomical analyses can inform anthropological research and illustrates the benefit of multidisciplinary studies.
Methods: A systematic literature review was conducted following PRISMA (preferred reporting items for systematic reviews and meta-analyses) guidelines and included journal articles and texts that discussed attachment sites, muscle architecture, function, and sexual dimorphism of the soft tissues in of interest.
Results: A total of 804 publications were assessed with a final number of 64 relevant texts, including 53 primary scientific articles and 11 textbooks. Upper trapezius and sternocleidomastoid were the most widely studied, while longissimus capitis and the nuchal ligament were the least. Additionally, there was limited consistent data on muscle architecture, attachment site morphology (entheses), sexual dimorphism, and population variation in these studies.
Conclusion: This paper highlights the need for more detailed architectural and enthesis data from diverse sex and population groups, and interdisciplinary research that will improve understanding of sexual dimorphism in humans. This can be applicable in clinical anatomy when assessing injury rates between males and females, and in anthropology, when estimating sex from the skeleton.

References

  • 1. Buikstra JE, Ubelaker DH. Standards for data collection from human skeletal remains. Fayetteville: Arkansas Archeological Survey Research Series No. 44; 1994. p. 272.
  • 2. Klales AR, Ousley SD, Vollner JM. A revised method of sexing the human innominate using Phenice’s nonmetric traits and statistical methods. Am J Phys Anthropol 2012;149:104−14.
  • 3. Phenice TW. A newly developed visual method of sexing the os pubis. Am J Phys Anthropol 1969;30:297−301.
  • 4. Walker PL. Sexing skulls using discriminant function analysis of visually assessed traits. Am J Phys Anthropol 2008;136:39−50.
  • 5. White TD, Black MT, Folkens PA. Human osteology. 3rd ed. San Diego (CA): Elsevier Science & Technology; 2011. p. 688.
  • 6. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hrobjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;10372:n71.
  • 7. Flack NA, Nicholson HD, Woodley SJ. A review of the anatomy of the hip abductor muscles, gluteus medius, gluteus minimus, and tensor fascia lata. Clin Anat 2012;25:697−708.
  • 8. Houseman ND, Taylor GI, Pan WR. The angiosomes of the head and neck: anatomic study and clinical applications. Plast Reconstr Surg 2000;105:2287−313.
  • 9. Humphreys BK, Kenin S, Hubbard BB, Cramer GD. Investigation of connective tissue attachments to the cervical spinal dura mater. Clin Anat 2003;16:152−9.
  • 10. Johnson G, Bogduk N, Nowitzke A, House D. Anatomy and actions of the trapezius muscle. Clin Biomech (Bristol, Avon) 1994;9:44−50.
  • 11. Mercer SR, Bogduk N. Clinical anatomy of ligamentum nuchae. Clin Anat 2003;16:484−93.
  • 12. Gray H. Anatomy, descriptive and surgical. London: John W. Parker and Son, West Strand; 1858.
  • 13. Standring S. Gray’s anatomy: the anatomical basis of clinical practice. 42nd ed. New York: Elsevier Limited; 2021. p. 1606.
  • 14. Rankin G, Stokes M, Newham DJ. Size and shape of the posterior neck muscles measured by ultrasound imaging: normal values in males and females of different ages. Man Ther 2005;10:108−15.
  • 15. Mayoux-Benhamou MA, Revel M, Wybier M, Barbet JP. Computerized tomographical study of dorsal neck muscles for insertion of EMG wire electrodes. J Electromyogr Kinesiol 1995;5:101− 7.
  • 16. Sinnatamby CS, Last RJ. Last’s anatomy: regional and applied. 12th ed. Edinburgh/New York: Churchill Livingstone/Elsevier; 2011. p. 560.
  • 17. Kamibayashi LK, Richmond FJ. Morphometry of human neck muscles. Spine (Phila Pa 1976) 1998;23:1314−23.
  • 18. Borst J, Forbes PA, Happee R, Veeger DH. Muscle parameters for musculoskeletal modelling of the human neck. Clin Biomech (Bristol, Avon) 2011;26:343−51.
  • 19. Bayoglu R, Geeraedts L, Groenen KHJ, Verdonschot N, Koopman B, Homminga J. Twente spine model: a complete and coherent dataset for musculo-skeletal modeling of the thoracic and cervical regions of the human spine. J Biomech 2017;58:52−63.
  • 20. Vasavada A, Ward S, Delp S, Lieber R. Architectural design and function of human back muscles. In: Herkowitz HN GS, Eismont FJ, Bell JR, Balderston RA, editors. The spine. 6th ed. Philadelphia (PA): Elsevier; 2011. p. 59−68.
  • 21. Knox R. A System of human anatomy on the basis of the “Traité D’Anatomie Descriptive” of M.H. Cloquet. 2nd ed. Edinburgh: Maclachlan and Stewart; 1831.
  • 22. Hansen JT, Netter FH, Machado CAG. Netter’s clinical anatomy. 4th ed. Philadelphia (PA): Elsevier; 2019. p. 588.
  • 23. Fielding JW, Burstein AH, Frankel VH. The nuchal ligament. Spine (Phila Pa 1976) 1976;1:3−14.
  • 24. Rea P. Neck. In: Rea P, editor. Essential clinically applied anatomy of the peripheral nervous system in the head and neck. Amsterdam: Academic Press; 2016. p. 131−83.
  • 25. Allia P, Gorniak G. Human ligamentum nuchae in the elderly: its function in the cervical spine. Journal of Manual and Manipulative Therapy 2013;14:11−21.
  • 26. Abbott LC, Lucas DB. The function of the clavicle: its surgical significance. Ann Surg 1954;140:583−99.
  • 27. Giacomo GD, Pouliart N, Costantini A, Vita AD. Atlas of functional shoulder anatomy. Milano: Springer; 2008. p. 231.
  • 28. Kawtharani FI, Hasan SS. Anatomy of the clavicle and its articulations. In: Groh GI, editor. Clavicle injuries. A case based guide to diagnosis and treatment. Cham, Switzerland: Springer International Publishing; 2018. Chapter 1; p. 1−17.
  • 29. Phadnis J, Bain GI. Clavicle anatomy. In: Bain GI, Itoi E, Di Giacomo G, Sugaya H, editors. Normal and pathological anatomy of the shoulder. Berlin, Heidelberg: Springer; 2015. Chapter 8; p. 71− 80.
  • 30. Frazer JE. The anatomy of the human skeleton. 2nd ed. London: J & A Churchill; 1920. p. 284.
  • 31. Klein Breteler MD, Spoor CW, Van der Helm FC. Measuring muscle and joint geometry parameters of a shoulder for modeling purposes. J Biomech 1999;32:1191−7.
  • 32. Van Ee CA, Nightingale RW, Camacho DL, Chancey VC, Knaub KE, Sun EA, Myers BS. Tensile properties of the human muscular and ligamentous cervical spine. Stapp Car Crash J 2000;44:85−102.
  • 33. Li F, Laville A, Bonneau D, Laporte S, Skalli W. Study on cervical muscle volume by means of three-dimensional reconstruction. J Magn Reson Imaging 2014;39:1411−6.
  • 34. Dawson RM, Latif Z, Haacke EM, Cavanaugh JM. Magnetic resonance imaging-based relationships between neck muscle cross-sectional area and neck circumference for adults and children. Eur Spine J 2013;22:446−52.
  • 35. Franklin D, Freedman L, Milne N, Oxnard CE. A geometric morphometric study of sexual dimorphism in the crania of indigenous southern Africans. South African Journal of Science 2006;102:229−38.
  • 36. Valera-Calero JA, Gallego-Sendarrubias G, Fernandez-de-Las-Penas C, Cleland JA, Ortega-Santiago R, Arias-Buria JL. Cross-sectional area of the cervical extensors assessed with panoramic ultrasound imaging: preliminary data in healthy people. Musculoskelet Sci Pract 2020;50:102257.
  • 37. Rezasoltani A, Kallinen M, Malkia E, Vihko V. Neck semispinalis capitis muscle size in sitting and prone positions measured by real-time ultrasonography. Clin Rehabil 1998;12:36−44.
  • 38. Elliott JM, Cornwall J, Kennedy E, Abbott R, Crawford RJ. Towards defining muscular regions of interest from axial magnetic resonance imaging with anatomical cross-reference: part II - cervical spine musculature. BMC Musculoskelet Disord 2018;19:171.
  • 39. Reddy C, Zhou Y, Wan B, Zhang X. Sex and posture dependence of neck muscle size-strength relationships. J Biomech 2021;127: 110660.
  • 40. Rezasoltani A, Nasiri R, Faizei AM, Zaafari G, Mirshahvelayati AS, Bakhshidarabad L. The variation of the strength of neck extensor muscles and semispinalis capitis muscle size with head and neck position. J Bodyw Mov Ther 2013;17:200−3.
  • 41. Uthaikhup S, Assapun J, Kothan S, Watcharasaksilp K, Elliott JM. Structural changes of the cervical muscles in elder women with cervicogenic headache. Musculoskelet Sci Pract 2017;29:1−6.
  • 42. Johnson GM, Zhang M, Jones DG. The fine connective tissue architecture of the human ligamentum nuchae. Spine (Phila Pa 1976) 2000;25:5−9.
  • 43. Kadri PAS, Al-Mefty O. Anatomy of the nuchal ligament and its surgical applications. Neurosurgery 2007;61:301−4.
  • 44. Ono A, Tonosaki Y, Numasawa T, Wada K, Yamasaki Y, Tanaka T, Kumagai G, Aburakawa S, Takeuchi K, Yokoyama T, Ueyama K, Ishibashi Y, Toh S. The relationship between the anatomy of the nuchal ligament and postoperative axial pain after cervical laminoplasty: cadaver and clinical study. Spine (Phila Pa 1976) 2012;37:E1607−13.
  • 45. Mitchell BS, Humphreys BK, O’Sullivan E. Attachments of the ligamentum nuchae to cervical posterior spinal dura and the lateral part of the occipital bone. J Manipulative Physiol Ther 1998;21:145−8.
  • 46. Takeshita K, Peterson ET, Bylski-Austrow D, Crawford AH, Nakamura K. The nuchal ligament restrains cervical spine flexion. Spine (Phila Pa 1976) 2004;29:E388−93.
  • 47. Dean NA, Mitchell BS. Anatomic relation between the nuchal ligament (ligamentum nuchae) and the spinal dura mater in the craniocervical region. Clin Anat 2002;15:182−5.
  • 48. Nash L, Nicholson H, Lee AS, Johnson GM, Zhang M. Configuration of the connective tissue in the posterior atlanto-occipital interspace: a sheet plastination and confocal microscopy study. Spine (Phila Pa 1976) 2005;30:1359−66.
  • 49. Zheng N, Yuan XY, Li YF, Chi YY, Gao HB, Zhao X, Yu SB, Sui HJ, Sharkey J. Definition of the to be named ligament and vertebrodural ligament and their possible effects on the circulation of CSF. PLOS One 2014;9:e103451.
  • 50. Kennedy E, Albert M, Nicholson H. The fascicular anatomy and peak force capabilities of the sternocleidomastoid muscle. Surg Radiol Anat 2017;39:629−45.
  • 51. Clark BS, Shah S, Chambers T. The sternocleidomastoid flap. Operative Techniques in Otolaryngology-Head and Neck Surgery 2019;30:138−44.
  • 52. Saha A, Mandal S, Chakraborty S, Bandyopadhyay M. Morphological study of the attachment of sternocleidomastoid muscle. Singapore Med J 2014;55:45−7.
  • 53. Ferreira-Arquez H. Multi headed sternocleidomastoid muscle: an anatomical study. International Journal of Pharma and Bio Sciences 2018;9:b249−56.
  • 54. Lee JT, Campbell KJ, Michalski MP, Wilson KJ, Spiegl UJ, Wijdicks CA, Millett PJ. Surgical anatomy of the sternoclavicular joint: a qualitative and quantitative anatomical study. J Bone Joint Surg Am 2014;96:e166.
  • 55. Alsalaheen B, Johns K, Bean R, Almeida A, Eckner J, Lorincz M. Women and men use different strategies to stabilize the head in response to impulsive loads: implications for concussion injury risk. J Orthop Sports Phys Ther 2019;49:779−86.
  • 56. de Amorim AA, Lins CCDA, Cardoso APD, Damascena CG. Variation in clavicular origin of sternocleidomastoid muscle. A case report. Int J Morphol 2010;28:97−8.
  • 57. Cherian SB, Nayak S. A rare case of unilateral third head of sternocleidomastoid muscle. Int J Morphol 2008;26:99−101.
  • 58. Dupont G, Iwanaga J, Altafulla JJ, Lachkar S, Oskouian RJ, Tubbs RS. Bilateral sternocleidomastoid variant with six distinct insertions along the superior nuchal line. Anat Cell Biol 2018;51:305−8.
  • 59. Fazliogullari Z, Cicekcibasi AE, Unver Dogan N, Yilmaz MT, Buyukmumcu M, Ziylan T. The levator claviculae muscle and unilateral third head of the sternocleidomastoid muscle: case report. Int J Morphol 2010;28:929−32.
  • 60. Heo YR, Kim JW, Lee JH. Variation of the sternocleidomastoid muscle: a case report of three heads and an accessory head. Surg Radiol Anat 2020;42:711−3.
  • 61. Kim SY, Jang HB, Kim J, Yoon SP. Bilateral four heads of the sternocleidomastoid muscle. Surg Radiol Anat 2015;37:871−3.
  • 62. Natsis K, Asouchidou I, Vasileiou M, Papathanasiou E, Noussios G, Paraskevas G. A rare case of bilateral supernumerary heads of sternocleidomastoid muscle and its clinical impact. Folia Morphol (Warsz) 2009;68:52−4.
  • 63. Oh JS, Kim CE, Kim J, Yoon SP. Bilateral supernumerary clavicular heads of sternocleidomastoid muscle in a Korean female cadaver. Surg Radiol Anat 2019;41:699−702.
  • 64. Raikos A, Paraskevas GK, Triaridis S, Kordali P, Psillas G, Brand-Saberi B. Bilateral supernumerary sternocleidomastoid heads with critical narrowing of the minor and major supraclavicular fossae: Clinical and surgical implications. Int J Morphol 2012;30:927−933.
  • 65. Sirasanagandla SR, Bhat KMR, Pamidi N, Somayaji SN. Unusual third head of the sternocleidomastoid muscle from the investing layer of cervical fascia. Int J Morphol 2012;30:783−5.
  • 66. Anıl A, Yasar YK, Anıl F, Coskun ZK, Peker T. Variation of bilateral multiheaded sternocleidomastoid muscle. Gazi Medical Journal 2017;28:56−7.
  • 67. Keidan L, Barash A, Lenzner Z, Pick CG, Been E. Sexual dimorphism of the posterior cervical spine muscle attachments. J Anat 2021;239:589−601.
  • 68. De Loose V, Van den Oord M, Keser I, Burnotte F, Van Tiggelen D, Dumarey A, Cagnie B, Witvrouw E, Danneels L. MRI study of the morphometry of the cervical musculature in F-16 pilots. Aviat Space Environ Med 2009;80:727−31.
  • 69. Elliott JM, Pedler AR, Jull GA, Van Wyk L, Galloway GG, O’Leary SP. Differential changes in muscle composition exist in traumatic and nontraumatic neck pain. Spine (Phila Pa 1976) 2014;39:39−47.
  • 70. Benjamin M, Toumi H, Ralphs JR, Bydder G, Best TM, Milz S. Where tendons and ligaments meet bone: attachment sites (‘entheses’) in relation to exercise and/or mechanical load. J Anat 2006; 208:471−90.
  • 71. Villotte S, Knusel CJ. Understanding entheseal changes: definition and life course changes. International Journal of Osteoarchaeology 2013;23:135−46.
  • 72. Kim BS, Kim DS, Kang S, Kim JY, Kang B, Rhyu IJ, Yoon JS. Ultrasound-guided injection of the sternocleidomastoid muscle: a cadaveric study with implications for chemodenervation. PM R 2021;13:503−9.
  • 73. Botticchio A, Mourad F, Fernandez-Carnero S, Arias-Buria JL, Santodomingo Bueno A, Mesa Jimenez J, Gobbo M. Short-term morphological changes in asymptomatic perimandibular muscles after dry needling assessed with rehabilitative ultrasound imaging: a proof-of-concept study. J Clin Med 2021;10:209−19.
There are 73 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Reviews
Authors

Jade S. De La Paz This is me 0000-0002-4190-7835

Hallie R. Buckley This is me 0000-0003-1047-4288

Siân E. Halcrow This is me 0000-0001-6038-7997

Stephanie J. Woodley This is me 0000-0002-7288-0209

Early Pub Date May 9, 2023
Publication Date August 30, 2022
Published in Issue Year 2022 Volume: 16 Issue: 2

Cite

APA De La Paz, J. S., Buckley, H. R., Halcrow, S. E., Woodley, S. J. (2022). A review of the anatomy of soft tissues associated with sexually dimorphic landmarks on the cranium. Anatomy, 16(2), 93-107.
AMA De La Paz JS, Buckley HR, Halcrow SE, Woodley SJ. A review of the anatomy of soft tissues associated with sexually dimorphic landmarks on the cranium. Anatomy. August 2022;16(2):93-107.
Chicago De La Paz, Jade S., Hallie R. Buckley, Siân E. Halcrow, and Stephanie J. Woodley. “A Review of the Anatomy of Soft Tissues Associated With Sexually Dimorphic Landmarks on the Cranium”. Anatomy 16, no. 2 (August 2022): 93-107.
EndNote De La Paz JS, Buckley HR, Halcrow SE, Woodley SJ (August 1, 2022) A review of the anatomy of soft tissues associated with sexually dimorphic landmarks on the cranium. Anatomy 16 2 93–107.
IEEE J. S. De La Paz, H. R. Buckley, S. E. Halcrow, and S. J. Woodley, “A review of the anatomy of soft tissues associated with sexually dimorphic landmarks on the cranium”, Anatomy, vol. 16, no. 2, pp. 93–107, 2022.
ISNAD De La Paz, Jade S. et al. “A Review of the Anatomy of Soft Tissues Associated With Sexually Dimorphic Landmarks on the Cranium”. Anatomy 16/2 (August 2022), 93-107.
JAMA De La Paz JS, Buckley HR, Halcrow SE, Woodley SJ. A review of the anatomy of soft tissues associated with sexually dimorphic landmarks on the cranium. Anatomy. 2022;16:93–107.
MLA De La Paz, Jade S. et al. “A Review of the Anatomy of Soft Tissues Associated With Sexually Dimorphic Landmarks on the Cranium”. Anatomy, vol. 16, no. 2, 2022, pp. 93-107.
Vancouver De La Paz JS, Buckley HR, Halcrow SE, Woodley SJ. A review of the anatomy of soft tissues associated with sexually dimorphic landmarks on the cranium. Anatomy. 2022;16(2):93-107.

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