Anatomy and Cell Biology

Korean Association of Anatomists (대한해부학회)
권호 표지
DOI QR코드

DOI QR Code

Development and cross-sectional morphology of the recurrent laryngeal nerves in human fetuses

  • Received : 2024.02.24
  • Accepted : 2024.05.09
  • Published : 2024.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

The recurrent laryngeal nerve is a bilateral branch of the vagus nerve that is mainly associated with the motor innervation of the intrinsic muscles of the larynx. Despite its bilateral distribution, the right and left recurrent laryngeal nerves display unequal length due to embryological processes related to the development of the aortic arches. This length asymmetry leads to theories about morphological compensations to provide symmetrical functions to the intrinsic muscles of the larynx. In this study we investigated the developmental and cross-sectional morphometrics of the recurrent laryngeal nerves in human fetuses. Fifteen stillbirth fetuses donated to anatomical and medical research were used for investigation. Fetuses had intrauterine age ranging from 30 to 40 weeks estimated by biometry methods. Specialized anatomical dissection of the visceral block of the neck was performed to prepare histological samples of the recurrent laryngeal nerves in its point of contact with the larynx, and morpho-quantitative techniques were applied to evaluate the epineurium and perineural space of the recurrent laryngeal nerves. No statistical difference in the cross-sectional morphology of the epineurium and perineural space between right and left recurrent laryngeal nerves intra-individually was confirmed, however, we found evidence that these structures are under greater development in the left recurrent laryngeal nerve during 30 to 40 weeks of intrauterine life. Our data suggest that the nerves are under morphological development that possibly set the stage for accommodation of larger diameter and myelinization of the left recurrent laryngeal nerve during post-natal life.

Keywords

Acknowledgement

We thank and appreciate the research support from the histology and anatomy technicians in the Department of Morphology at the Federal University of the Espirito Santo. We acknowledge and sincerely thank the families of the donors for their altruistic act in favor of medical science and anatomical research. These donors and their families deserve our highest gratitude.

References

  1. Damste PH. The larynx as a wind-instrument. Pract Otorhinolaryngol (Basel) 1965;27:94-5.
  2. Saito S, Fukuda H, Kitahara S, Kokawa N. Stroboscopic observation of vocal fold vibration with fiberoptics. Folia Phoniatr (Basel) 1978;30:241-4. https://doi.org/10.1159/000264132
  3. Gardner ED, O'Rahilly R, Muller F. Gardner-Gray-O'Rahilly anatomy: a regional study of human structure. 5th ed. Saunders; 1986.
  4. Dalley AF, Agur AMR. Moore's clinically oriented anatomy. 9th ed. Wolters Kluwer Health; 2021.
  5. Maranillo E, de Blas CS, Gorriz MC, Quinones S, Verdu E, Quer M, Leon X, Vazquez T, Sanudo JR, Konschake M. Comparative study of the length of human laryngeal nerves and their variations: functional and clinical considerations. Eur J Anat 2021;25:653-63.
  6. Prades JM, Dubois MD, Dumollard JM, Tordella L, Rigail J, Timoshenko AP, Peoc'h M. Morphological and functional asymmetry of the human recurrent laryngeal nerve. Surg Radiol Anat 2012;34:903-8.
  7. Valenzuela-Fuenzalida JJ, Baeza-Garrido V, Navia-Ramirez MF, Cariseo-Avila C, Bruna-Mejias A, Becerra-Farfan A, Lopez E, Orellana Donoso M, Loyola-Sepulveda W. Systematic review and meta-analysis: recurrent laryngeal nerve variants and their implication in surgery and neck pathologies, using the anatomical quality assurance (AQUA) checklist. Life (Basel) 2023;13:1077.
  8. Atkins JP Jr. An electromyographic study of recurrent laryngeal nerve conduction and its clinical applications. Laryngoscope 1973;83:796-807. https://doi.org/10.1288/00005537-197305000-00015
  9. Pascual-Font A, Merchan A, Maranillo E, Brillas A, Sanudo JR, Valderrama-Canales FJ. [Morphometry of the recurrent laryngeal nerves of the rat]. Acta Otorrinolaringol Esp 2006;57:435-40. Spanish. https://doi.org/10.1016/S0001-6519(06)78744-1
  10. Patel RR, Awan SN, Barkmeier-Kraemer J, Courey M, Deliyski D, Eadie T, Paul D, Svec JG, Hillman R. Recommended protocols for instrumental assessment of voice: American SpeechLanguage-Hearing Association expert panel to develop a protocol for instrumental assessment of vocal function. Am J Speech Lang Pathol 2018;27:887-905. https://doi.org/10.1044/2018_AJSLP-17-0009
  11. Harrison DF. Fibre size frequency in the recurrent laryngeal nerves of man and giraffe. Acta Otolaryngol 1981;91:383-9. https://doi.org/10.3109/00016488109138519
  12. Shin T, Rabuzzi DD. Conduction studies of the canine recurrent laryngeal nerve. Laryngoscope 1971;81:586-96. https://doi.org/10.1288/00005537-197104000-00010
  13. March MI, Warsof SL, Chauhan SP. Fetal biometry: relevance in obstetrical practice. Clin Obstet Gynecol 2012;55:281-7. https://doi.org/10.1097/GRF.0b013e3182446e9b
  14. Streeter GL. Weight, sitting height, head size, foot length, and menstrual age of the human embryo. Carnegie Inst Wash 1920;11:143-79.
  15. Kinoshita H, Umezawa T, Omine Y, Kasahara M, Rodriguez-Vazquez 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. https://doi.org/10.5115/acb.2013.46.1.39
  16. Mallory FB. A contribution to staining methods: I. A differential stain for connective-tissue fibrillae and reticulum. II. Chloride of iron haematoxylin for nuclei and fibrin. III. Phosphotungstic acid haematoxylin for neuroglia fibres. J Exp Med 1900;5:15-20. https://doi.org/10.1084/jem.5.1.15
  17. Sadler TW. Langman's medical embryology. 15th ed. Wolters Kluwer; 2024.
  18. World Health Organization. Stillbirth [Internet]. World Health Organization; c2024 [cited 2024 Apr 4]. Available from: https://www.who.int/health-topics/stillbirth
  19. Aminu M, Bar-Zeev S, van den Broek N. Cause of and factors associated with stillbirth: a systematic review of classification systems. Acta Obstet Gynecol Scand 2017;96:519-28. https://doi.org/10.1111/aogs.13126
  20. Naidu L, Lazarus L, Partab P, Satyapal KS. Laryngeal nerve "anastomoses". Folia Morphol (Warsz) 2014;73:30-6. https://doi.org/10.5603/FM.2014.0005
  21. Henry BM, Pekala PA, Sanna B, Vikse J, Sanna S, Saganiak K, Tomaszewska IM, Tubbs RS, Tomaszewski KA. The anastomoses of the recurrent laryngeal nerve in the larynx: a metaanalysis and systematic review. J Voice 2017;31:495-503. https://doi.org/10.1016/j.jvoice.2016.11.004
  22. Ellwanger JH, da Costa Rosa JP, dos Santos IP, da Rosa HT, Jotz GP, Xavier LL, de Campos D. Morphologic evaluation of the fetal recurrent laryngeal nerve and motor units in the thyroarytenoid muscle. J Voice 2013;27:668-73. https://doi.org/10.1016/j.jvoice.2013.07.004
  23. Jotz GP, de Campos D, Rodrigues MF, Xavier LL. Histological asymmetry of the human recurrent laryngeal nerve. J Voice 2011;25:8-14.
  24. Harding R. Function of the larynx in the fetus and newborn. Annu Rev Physiol 1984;46:645-59. https://doi.org/10.1146/annurev.ph.46.030184.003241
  25. Fleming JC, Gibbins N, Ingram PJ, Harries M. An anatomical study of the myelination of human laryngeal nerves. J Laryngol Otol 2011;125:1263-7. https://doi.org/10.1017/S0022215111001939
  26. Wozniak W, O'Rahilly R. Fine structure and myelination of the developing human vagus nerve. Acta Anat (Basel) 1981;109:218-30. https://doi.org/10.1159/000145387
  27. Tanaka S, Mito T, Takashima S. Progress of myelination in the human fetal spinal nerve roots, spinal cord and brainstem with myelin basic protein immunohistochemistry. Early Hum Dev 1995;41:49-59. https://doi.org/10.1016/0378-3782(94)01608-R
  28. Standring S, Gray H. Gray's anatomy: the anatomical basis of clinical practice. 42nd ed. Elsevier; 2021. 1588 p.
  29. Lanigan LG, Russell DS, Woolard KD, Pardo ID, Godfrey V, Jortner BS, Butt MT, Bolon B. Comparative pathology of the peripheral nervous system. Vet Pathol 2021;58:10-33. https://doi.org/10.1177/0300985820959231
  30. Brown IS. Pathology of perineural spread. J Neurol Surg B Skull Base 2016;77:124-30. https://doi.org/10.1055/s-0036-1571837
  31. Crowe TP, Greenlee MHW, Kanthasamy AG, Hsu WH. Mechanism of intranasal drug delivery directly to the brain. Life Sci 2018;195:44-52. https://doi.org/10.1016/j.lfs.2017.12.025
  32. Shanthaveerappa TR, Bourne GH. Perineural epithelium: a new concept of its role in the integrity of the peripheral nervous system. Science 1966;154:1464-7. https://doi.org/10.1126/science.154.3755.1464