Skip to main content

Advertisement

SpringerLink
Log in

Submucosal Elastic Laminae of the Middle and Lower Pharynx: A Histological Study Using Elderly Cadaveric Specimens

  • Original Article
  • Published:
Dysphagia Aims and scope Submit manuscript

Abstract

Although the pharyngeal wall is well known to have high elasticity, the distribution of submucosal elastic fibers has not been described. Observations of histological sections of the mid and lower pharyngeal walls from 15 elderly donated cadavers were made. We found two distinct submucosal tissue layers with a high content of elastic fibers (tentatively termed the “submucosal elastic laminae”). The inferolateral elastic lamina was restricted to the level from the upper part of the arytenoid to the lower end of the inferior cornu of the thyroid cartilage. It originated from the pharyngeal submucosa, extended laterally along the inner aspect of the thyropharyngeal muscle, and inserted into the posterior margin of the thyroid cartilage including the cornu. The posteromedial lamina extended along the supero-inferior axis from a level above the greater horn of the hyoid bone to reach the muscularis mucosae of the cervical esophagus. The inferolateral and posteromedial laminae were connected at levels below the cricoarytenoid joint. Individual variations were evident in their thicknesses (ranging from almost absent to 0.3 mm) as well as the extent of connection between them. In association with striated muscle function, the inferolateral lamina seemed to suspend the lower pharyngeal mucosa, while the posteromedial lamina seemed to provide mucosal fold forcing smoothly peristaltic conveyance of a bolus during swallowing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Nishikubo K, Mise K, Ameya M, Hirose K, Kobayashi T, Hyodo M. Quantitative evaluation of age-related alteration of swallowing function: videofluoroscopic and manometric studies. Auris Nasus Larynx. 2015;42(2):134–8.

    Article  PubMed  Google Scholar 

  2. Im I, Kim Y, Oommen E, Kim H, Ko MH. The effects of bolus consistency in pharyngeal transit duration during normal swallowing. Ann Rehabil Med. 2012;36(2):220–5.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Leonard R, Kendall K, McKenzie S. UES opening and cricopharyngeal bar in nondysphagic elderly and nonelderly adults. Dysphagia. 2004;19(3):182–91.

    Article  PubMed  Google Scholar 

  4. Roberts TJ. Contribution of elastic tissues to the mechanics and energetics of muscle function during movement. J Exp Biol. 2016;219(Pt 2):266–75.

    Article  PubMed  Google Scholar 

  5. Sivarao DV, Goyal RK. Functional anatomy and physiology of the upper esophageal sphincter. Am J Med. 2000;108(suppl 4a):27S–37S.

    Article  PubMed  Google Scholar 

  6. Kinoshita H, Umezawa T, Omine Y, Kasahara M, Rodríguez-Vázquez JF, Murakami G, Abe S. Distribution of elastic fibers in the head and neck: a histological study using late-stage human fetuses. Anat Cell Biol. 2013;46:39–48.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hinata N, Murakami G. The urethral rhabdosphincter, levator ani muscle and perineal membrane: a review. BioMed Res Int. 2014;2014:906921.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kim JH, Kinugasa Y, Yu HC, Murakami G, Abe S, Cho BH. Lack of striated muscle fibers in the longitudinal anal muscle of elderly Japanese: a histological study using cadaveric specimens. Int J Colorectal Dis. 2015;30:43–9.

    Article  PubMed  Google Scholar 

  9. Bosma JF, Bartner H. Ligaments of the larynx and the adjacent pharynx and esophagus. Dysphagia. 1993;8:23–8.

    Article  CAS  PubMed  Google Scholar 

  10. Wang Q, Xu S, Tu L, Zhang M. Anatomic continuity of longitudinal pharyngeal and esophageal muscles. Laryngoscope. 2007;117:282–7.

    Article  PubMed  Google Scholar 

  11. Motohashi O, Suzuki M, Shida N, Umezawa T, Ohtoh Y, Sakurai Y, Yoshimoto T. Subarachnoid heamorrhage induced proliferation of leptomeningeal cells and deposition of extracellular matricies in the arachnoid granulations and subarachnoid space. Acta Neurochir. 1995;136:88–91.

    Article  CAS  PubMed  Google Scholar 

  12. Okada R, Arima K, Kawai M. Arterial changes in cerebral autosomal dominant arteriopathy with subbcortical infarcts and leukoencephalopathy (CADASIL) in relation to pathogenesis of diffuse myelin loss of cerebral white matter. Stroke. 2002;33:2565–9.

    Article  Google Scholar 

  13. Hayashi S, Murakami G, Ohtsuka A, Itoh M, Nakano T, Fukuzawa Y. Connective tissue configuration in the human liver hilar region with special reference to the liver capsule and vascular sheath. J Hepatobiliary Pancreat Surg. 2008;15:640–7.

    Article  PubMed  Google Scholar 

  14. Ohtuka K, Tomita H, Murakami G. Anatomy of the tonsilar bed: topographical relationship between the palatine tonsil and the lingual branch of the glossopharyngeal nerve. Acta Orolaryngol suppl. 2002;546:99–109.

    Article  Google Scholar 

  15. Han M, Murakami G, Suzuki D, Miyamoto S. Anatomical variations in stylopharyngeus muscle insertions suggest interindividual and left/right differences in pharyngeal clearance function of elderly patients: a cadaveric study. Dysphagia. 2008;23:251–7.

    Article  Google Scholar 

  16. Sakamoto Y. Spatial relationship between the palatopharyngeus and the superior constrictor of the pharynx. Surg Radiol Anat. 2015;37:649–55.

    Article  PubMed  Google Scholar 

  17. Gates GA. Upper esophageal sphincter: pre and post-laryngectomy.-a normative study. Laryngoscope. 1980;90:454–64.

    Article  CAS  PubMed  Google Scholar 

  18. Lang IM, Shaker R. An overview of the upper esophageal sphincter. Curr Gastroenterol Rep. 2000;2:185–90.

    Article  CAS  PubMed  Google Scholar 

  19. Kahrilas PJ, Dodds WJ, Dent J, Logemann JA, Shaker R. Upper esophageal sphincter function during deglutition. Gastroenterol. 1988;95:52–62.

    Article  CAS  Google Scholar 

  20. Cook IJ, Dodds WJ, Dantas RO, Massey B, Kern MK, Lang IM, Brasseur JG, Hogan WJ. Opening mechanisms of the human upper esophageal sphincter. Am J Physiol. 1989;257:G748–59.

    CAS  PubMed  Google Scholar 

  21. Jacob P, Kahrilas PJ, Logemann JA, Shah V. Hat: upper esophageal sphincter opening and modulation during swallowing. Gastroenterol. 1989;97:1469–78.

    Article  CAS  Google Scholar 

  22. Kern M, Bardan E, Arndorfer R, Hofmann C, Ren J, Shaker R. Comparison of upper esophageal sphincter opening in healthy asymptomatic young and elderly volunteers. Ann Otol Rhinol Laryngol. 1999;108(10):982–9.

    Article  CAS  PubMed  Google Scholar 

  23. Cook IJ, Blumbergs P. cash K, Jamieson GG, Shearman DJ: structural abnormalities of the cricopharyngeus muscle in patients with pharyngeal (Zenker’s) diverticulum. J Gastroenterol Hepatol. 1992;7:556–62.

    Article  CAS  PubMed  Google Scholar 

  24. Taguchi A, Hyodo M, Yamagata T, Gyo K, Desaki J. Age-related remodeling of the hypopharyngeal constrictor muscle and its subneural apparatuses: a scanning electron microscopical study in rats. Dysphagia. 2004;19(4):241–7.

    Article  PubMed  Google Scholar 

  25. Bonta M, Daina L, Muţiu G. The process of ageing reflected by histological changes in the skin. Rom J Morphol Embryol. 2013;54(3 Suppl):797–804.

    PubMed  Google Scholar 

  26. Sato K, Shirouzu H, Nakashima T. Irradiated macula flava in the human vocal fold mucosa. Am J Otolaryngol. 2008;29(5):312–8.

    Article  PubMed  Google Scholar 

  27. Fukuda Y, Ferrans VJ. Pulmonary elastic fiber degradation in paraquat toxicity. An electron microscopic immunohistochemical study. J Submicrosc Cytol Pathol. 1988;20(1):15–23.

    CAS  PubMed  Google Scholar 

  28. Kawamoto-Hirano A, Honkura Y, Shibata S, Abe S, Murakami G, Katori Y. Cricoarytenoid articulation in elderly Japanese with special reference to morphology of the synovial and capsular tissues. Ann Otol Rhinol Laryngol. 2015;125(3):219–27.

    Article  PubMed  Google Scholar 

  29. Kawamoto A, Honkura Y, Suzuki R, Abe H, Murakami G, Katori Y: Cricothyroid articulation in Japanese elderly with special reference to morphology of the synovial and capsular tissues. J Voice: in press, 2015.

Download references

Acknowledgments

We are grateful to the individuals who donated their bodies after death to Tokyo Dental College for research and education on human anatomy without any economic benefit. We also thank their families for agreeing to the donation as well as their patience in waiting for the return of their remains after study.

Author information

Authors and Affiliations

  1. Department of Otolaryngology-Head and Neck Surgery, Tohoku University Graduate School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8574, Japan

    Ai Kawamoto-Hirano, Yohei Honkura & Yukio Katori

  2. Department of Anatomy, Tokyo Dental College, 2-9-18 Misakicho, Chiyoda-Ku, Tokyo, 101-0061, Japan

    Masahito Yamamoto & Shin-ichi Abe

  3. Division of Internal Medicine, Iwamizawa Asuka Hospital, 297-13, Shibuncho, Iwamizawa, Hokkaido, 068-0833, Japan

    Gen Murakami

Authors
  1. Ai Kawamoto-Hirano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yohei Honkura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masahito Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shin-ichi Abe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gen Murakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yukio Katori
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ai Kawamoto-Hirano.

Ethics declarations

Conflicts of interest

The authors declare that there is no conflict of interest associated with this manuscript.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kawamoto-Hirano, A., Honkura, Y., Yamamoto, M. et al. Submucosal Elastic Laminae of the Middle and Lower Pharynx: A Histological Study Using Elderly Cadaveric Specimens. Dysphagia 31, 635–643 (2016). https://doi.org/10.1007/s00455-016-9721-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-016-9721-y

Keywords

Search

Navigation