Anat Cell Biol.  2023 Sep;56(3):374-381. 10.5115/acb.23.081.

Histological observations of age-related changes in the epiglottis associated with decreased deglutition function in older adults

• Serikawa M
• Ambe K
• Usami A

• KMID: 2546466
• DOI: http://doi.org/10.5115/acb.23.081

Abstract

Although the epiglottis plays a vital role in deglutition, histological studies of the epiglottis and surrounding ligaments associated with swallowing dysfunction are limited. Therefore, we performed histological observations to clarify age-related changes in the morphological characteristics of the epiglottis and surrounding structures. Tissue samples comprising the epiglottis and surrounding structures were collected from corpses that were both orally fed and tubefed during their lifetimes. Following hematoxylin and eosin, Elastica Van Gieson, and immunohistochemical staining procedures, the chondrocytes, connective tissue, and glandular tissue were observed under the epiglottis epithelium, and intervening adipose tissue was observed in the surrounding area. Fatty degeneration of acinar cells was also observed in the glandular tissue, possibly because of aging. Bundles of elastic fibers were present around the vascular wall in the periepiglottic ligament, but some were reduced. Furthermore, large amounts of collagen fibers ran toward and through the cartilage, whereas the mesh-like elastic fibers stopped in front of the cartilage. Microfibrils considered to be oxytalan fibers, which are thinner and shorter than elastic fibers, were observed around the vascular wall and in the fiber bundles. Agerelated changes included connective tissue fibrosis shown by the large amount of collagen fibers, atrophy of salivary glands, and an accompanying increase in adipose tissue. Regarding stretchability and elasticity, the elastic fibers may have an auxiliary function for laryngeal elevation during deglutition. This suggests that disuse atrophy of the laryngeal organs with or without oral intake might reduce the amount of elastic fiber in older adults.

Keyword

Older adults; Epiglottis; Oxytalan fiber; Oral intake; Muscular disorders; atrophic

Figure

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  Fig. 1 Schematic diagrams of (A) the larynx (sagittal section), the enlarged view of the smaller rectangle corresponds to (B) and the enlarged view of the larger rectangle corresponds to (C). (B) the thyroepiglottic ligament, and (C) the hyoid-epiglottic ligament.

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  Fig. 2 Hematoxylin & eosin staining image under epiglottis epithelium (×4). (A) and (B) are stained images of different samples. The image in the lower right of (B) is a magnified portion of the glandular tissue (×40). Black scale bar: 200 μm and red scale bar: 100 μm. Red arrowheads indicate acinar tissues (fatty degeneration). AC, acinar cells (normal); BV, blood vessels; C, cartilage; F, fat; P, perichondrium.

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  Fig. 3 Elastica Van Gieson stained image near the thyroid cartilage in the thyroepiglottic ligament ([A] ×5, scale bar: 200 μm; [B] ×20, scale bar: 50 μm). Asterisks (*) indicate elastic fibers and arrowheads indicates collagen fibers. TC, thyroid cartilage.

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  Fig. 4 Elastica Van Gieson stained image of the hyoid–epiglottic ligament. (A) Fiber bundles running along the epiglottis (×10, scale bar: 100 μm), (B) near the hyoid bone (×20, scale bar: 50 μm), (C) near the center of the ligament (×20, scale bar: 50 μm), and (D) near the epiglottis (×20, scale bar: 50 μm). Asterisks (*) indicate elastic fibers and arrowheads indicate collagen fibers. EC, epiglottis; GT, glandular tissue; HB, hyoid bone; P, perichondrium.

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  Fig. 5 Elastica Van Gieson staining images of (A) near the hyoid bone (×5, scale bar: 200 μm), (B) enlarged image of the square part of (A) (×20, scale bar: 50 μm), (C) near the epiglottis (×10, scale bar: 100 μm), and (D) near the center of the ligament (×20, scale bar: 50 μm). Arrowheads indicate collagen fiber. BV, blood vessel; EC, epiglottis; GT, glandular tissue; HB, hyoid bone.

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  Fig. 6 (A) Immunohistochemical staining of factor VIII near the epiglottis (×20) and (B) immunohistochemical staining of factor VIII in ligamentous fibers (×20). Scale bar: 50 μm. Arrowheads indicate collagen fibers and red arrows indicate capillaries (factor VIII positive). EC, epiglottis.

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  Fig. 7 (A) Immunohistochemical staining image of fibrillin 1 in ligamentous fibers (×20). (B) Immunohistochemical staining image of fibrillin 1 around the blood vessel wall distributed in the epiglottis (×20). Scale bar: 50 μm. Arrowheads indicate collagen fiber and arrows indicate Fibrillin 1 antibody-positive site. BV, blood vessel.

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  Fig. 8 Immunohistochemical staining image of fibrillin 1 in the fiber group of the thyroepiglottic ligament (×20). Samples from (A) corpses capable of oral intake, and (B) corpses who relied on enteral nutrition. Red arrows indicate fibrillin 1 antibody-positive microfibrils, which are presumed to be oxytalan fibers. Scale bar: 100 μm.

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  Fig. 9 Immunohistochemical staining image of fibrillin 1 in the fiber group of the hyoid–epiglottic ligament (×20). Samples from (A) corpses capable of oral intake, and (B) corpses who relied on enteral nutrition. Red arrows indicate fibrillin 1 antibody-positive microfibrils, which are presumed to be oxytalan fibers. Scale bar: 100 μm.

Reference

References

1. Lamb J. 1974; Movements and functions of the epiglottis during deglutition. Edinb Dent Hosp Gaz. 13:22–30. PMID: 4532072.

2. Gleeson DC. 1999; Oropharyngeal swallowing and aging: a review. J Commun Disord. 32:373–95. quiz 395–6. DOI: 10.1016/S0021-9924(99)00017-9. PMID: 10560713.

3. Daniels SK, Corey DM, Hadskey LD, Legendre C, Priestly DH, Rosenbek JC, Foundas AL. 2004; Mechanism of sequential swallowing during straw drinking in healthy young and older adults. J Speech Lang Hear Res. 47:33–45. DOI: 10.1044/1092-4388(2004/004). PMID: 15072526.

4. Leonard R, Kendall KA, McKenzie S. 2004; Structural displacements affecting pharyngeal constriction in nondysphagic elderly and nonelderly adults. Dysphagia. 19:133–41. DOI: 10.1007/s00455-003-0508-6. PMID: 15382802.

5. Kang BS, Oh BM, Kim IS, Chung SG, Kim SJ, Han TR. 2010; Influence of aging on movement of the hyoid bone and epiglottis during normal swallowing: a motion analysis. Gerontology. 56:474–82. DOI: 10.1159/000274517. PMID: 20068282.

6. Satoda T, Shimoe S, Makihira S, Tamamoto M, Murayama T, Nikawa H. 2008; Model for the functional instruction of swallowing. Kaibogaku Zasshi. 83:51–7. Japanese. PMID: 18572803.

7. Standring S. 2016. Gray's anatomy: the anatomical basis of clinical practice. 41st ed. Elsevier;p. 583.

8. Tamine K, Ono T, Hori K, Kondoh J, Hamanaka S, Maeda Y. 2010; Age-related changes in tongue pressure during swallowing. J Dent Res. 89:1097–101. DOI: 10.1177/0022034510370801. PMID: 20530725.

9. Inamoto Y, Saitoh E, Okada S, Kagaya H, Shibata S, Baba M, Onogi K, Hashimoto S, Katada K, Wattanapan P, Palmer JB. 2015; Anatomy of the larynx and pharynx: effects of age, gender and height revealed by multidetector computed tomography. J Oral Rehabil. 42:670–7. DOI: 10.1111/joor.12298. PMID: 25892610.

10. Ximenes Filho JA, Tsuji DH, do Nascimento PH, Sennes LU. 2003; Histologic changes in human vocal folds correlated with aging: a histomorphometric study. Ann Otol Rhinol Laryngol. 112:894–8. DOI: 10.1177/000348940311201012. PMID: 14587982.

11. Kuhn MA. 2014; Histological changes in vocal fold growth and aging. Curr Opin Otolaryngol Head Neck Surg. 22:460–5. DOI: 10.1097/MOO.0000000000000108. PMID: 25232935.

12. Pellnitz D. 1961; On change in the morphology of the human epiglottis due to aging. Arch Ohren Nasen Kehlkopfheilkd. 178:350–4. German. DOI: 10.1007/BF02103223. PMID: 14484990.

13. Kano M, Shimizu Y, Okayama K, Igari T, Kikuchi M. 2005; A morphometric study of age-related changes in adult human epiglottis using quantitative digital analysis of cartilage calcification. Cells Tissues Organs. 180:126–37. DOI: 10.1159/000086753. PMID: 16113541.

14. JafariNasabian P, Inglis JE, Reilly W, Kelly OJ, Ilich JZ. 2017; Aging human body: changes in bone, muscle and body fat with consequent changes in nutrient intake. J Endocrinol. 234:R37–51. DOI: 10.1530/JOE-16-0603. PMID: 28442508.

15. Bender AD. 1965; The effect of increasing age on the distribution of peripheral blood flow in man. J Am Geriatr Soc. 13:192–8. DOI: 10.1111/j.1532-5415.1965.tb02665.x. PMID: 14270624.

16. Henninger HB, Ellis BJ, Scott SA, Weiss JA. 2019; Contributions of elastic fibers, collagen, and extracellular matrix to the multiaxial mechanics of ligament. J Mech Behav Biomed Mater. 99:118–26. DOI: 10.1016/j.jmbbm.2019.07.018. PMID: 31351401. PMCID: PMC7474469.

17. Gumpangseth T, Lekawanvijit S, Mahakkanukrauh P. 2020; Histological assessment of the human heart valves and its relationship with age. Anat Cell Biol. 53:261–71. DOI: 10.5115/acb.20.093. PMID: 32727956. PMCID: PMC7527117.

18. Yabe Y, Hagiwara Y, Tsuchiya M, Honda M, Hatori K, Sonofuchi K, et al. 2016; Decreased elastic fibers and increased proteoglycans in the ligamentum flavum of patients with lumbar spinal canal stenosis. J Orthop Res. 34:1241–7. DOI: 10.1002/jor.23130. PMID: 26679090.

19. Irvine LE, Yang Z, Kezirian EJ, Nimni ME, Han B. 2018; Hyoepiglottic ligament collagen and elastin fiber composition and changes associated with aging. Laryngoscope. 128:1245–8. DOI: 10.1002/lary.27094. PMID: 29330863.

20. Sawatsubashi M, Umezaki T, Kusano K, Tokunaga O, Oda M, Komune S. 2010; Age-related changes in the hyoepiglottic ligament: functional implications based on histopathologic study. Am J Otolaryngol. 31:448–52. DOI: 10.1016/j.amjoto.2009.08.003. PMID: 20015802.

21. Böck P. 1983; Elastic fiber microfibrils: filaments that anchor the epithelium of the epiglottis. Arch Histol Jpn. 46:307–14. DOI: 10.1679/aohc.46.307. PMID: 6685469.

22. Goldfischer S, Coltoff-Schiller B, Schwartz E, Blumenfeld OO. 1983; Ultrastructure and staining properties of aortic microfibrils (oxytalan). J Histochem Cytochem. 31:382–90. DOI: 10.1177/31.3.6186732. PMID: 6186732.

23. Strydom H, Maltha JC, Kuijpers-Jagtman AM, Von den Hoff JW. 2012; The oxytalan fibre network in the periodontium and its possible mechanical function. Arch Oral Biol. 57:1003–11. DOI: 10.1016/j.archoralbio.2012.06.003. PMID: 22784380.

24. Inoue K, Hara Y, Sato T. 2012; Development of the oxytalan fiber system in the rat molar periodontal ligament evaluated by light- and electron-microscopic analyses. Ann Anat. 194:482–8. DOI: 10.1016/j.aanat.2012.03.010. PMID: 22727934.

25. Giusti B, Pepe G. 2016; Fibrillins in tendon. Front Aging Neurosci. 8:237. DOI: 10.3389/fnagi.2016.00237. PMID: 27812333. PMCID: PMC5071311. PMID: 162c0652ed0e41b8a41caeef487c241b.

26. Barros EM, Rodrigues CJ, Rodrigues NR, Oliveira RP, Barros TE, Rodrigues AJ Jr. 2002; Aging of the elastic and collagen fibers in the human cervical interspinous ligaments. Spine J. 2:57–62. DOI: 10.1016/S1529-9430(01)00167-X. PMID: 14588289.

27. Rodrigues CJ, Rodrigues Junior AJ. 2000; A comparative study of aging of the elastic fiber system of the diaphragm and the rectus abdominis muscles in rats. Braz J Med Biol Res. 33:1449–54. DOI: 10.1590/S0100-879X2000001200008. PMID: 11105097. PMID: e778f79cdda84ec6936e12844aad744e.

28. Quintas ML, Rodrigues CJ, Yoo JH, Rodrigues Junior AJ. 2000; Age related changes in the elastic fiber system of the interfoveolar ligament. Rev Hosp Clin Fac Med Sao Paulo. 55:83–6. DOI: 10.1590/S0041-87812000000300003. PMID: 10983010.

29. Ramirez F, Pereira L. 1999; The fibrillins. Int J Biochem Cell Biol. 31:255–9. DOI: 10.1016/S1357-2725(98)00109-5. PMID: 10216958.

30. Finocchiaro E, Galletti R, Costantino A, Rivetti M, Xompero G, Aimonino N, Balzola F. 1992; Enteral nutrition in the elderly. Minerva Gastroenterol Dietol. 38:109–13. Italian. PMID: 1391146.

31. Nogami T, Kurachi M, Hukushi T, Iwasaki K. 2020; Recovery of oral feeding in Japanese elderly people after long-term tube feeding: a challenge in Miyama Hospital. J Family Med Prim Care. 9:3977–80. DOI: 10.4103/jfmpc.jfmpc_567_20. PMID: 33110796. PMCID: PMC7586527. PMID: b6969d91465847d1a381644d287b272f.

32. Katsume H, Furukawa K, Azuma A, Nakamura T, Matsubara K, Ohnishi K, Sugihara H, Asayama J, Nakagawa M. 1992; Disuse atrophy of the left ventricle in chronically bedridden elderly people. Jpn Circ J. 56:201–6. DOI: 10.1253/jcj.56.201. PMID: 1552647.

33. Wall BT, Dirks ML, van Loon LJ. 2013; Skeletal muscle atrophy during short-term disuse: implications for age-related sarcopenia. Ageing Res Rev. 12:898–906. DOI: 10.1016/j.arr.2013.07.003. PMID: 23948422.