Abstract
Background
There is no information about muscle growth in eyelids with infrequent blinking in fetuses.
Methods
To examine the muscle and nerve morphology, we morphometrically and immunohistochemically examined sagittal sections of unilateral upper eyelids obtained from 21 term fetuses (approximately 30–42 weeks of gestation) and, for the comparison, those from 10 midterm fetuses (12–15 weeks).
Results
The approximation margin of the upper eyelid always corresponded to the entire free margin in midterm fetuses, whereas it was often (18/21) restricted in the posterior part in term fetuses. Thus, in the latter, the thickness at the approximation site to the lower lid often ranged from 0.8 to 1.6 mm and corresponded to 18–56% of the nearly maximum thickness of the lid. In the lower part of the upper eyelid, a layer of the orbicularis oculi muscles often (14/21) provided posterior flexion at 90–120° to extend posteriorly. Nerve fibers running along the mediolateral axis were rich along the approximation surface at term, but they might not be reported in the upper eyelid of adults.
Conclusion
Being different from adult morphologies, the term eyelid was much thicker than the approximation surface and it carried a flexed muscle layer and transversely-running nerve. The infrequent blinking in fetuses seemed to provide a specific condition for the muscle-nerve growth. Plastic and pediatric surgeons should pay attention to a fact that infants’ upper eyelid was unlikely to be a mini-version of the adult morphology.
Similar content being viewed by others
Availability of data
Not applicable.
References
Bacharach J, Lee WW, Harrison AR et al (2021) A review of acquired blepharoptosis: prevalence, diagnosis, and current treatment options. Eye 35:2468–2481
Bron AJ, Tripathi RC, Tripathi BJ (1997) Eugene Wolff’s anatomy of the eye and orbit, 8th edn. Chapman & Hall Medical, London, pp 30–40
Byun TH, Kim JT, Park HW et al (2011) Timetable for upper eyelid development in staged human embryos and fetuses. Anat Rec 294:789–796
Cho KH, Jang HS, Abe H et al (2018) Fetal development of fasciae around the arm and thigh muscles: a study using late-stage fetuses. Anat Rec 301:1235–1243
Deady JP, Morrell AJ, Sutton GA (1989) Recognising aponeurotic ptosis. J Neurol Neurosurg Psychiatry 52:996–998
Evereklioglu C (2023) Frontalis suspension by a minimally invasive “harvesting-stripping technique” for congenital blepharoptosis in children under 3-years-old. Eur J Ophthalmol 33:161–170
Hayashi T, Kumasaka T, Mitani K et al (2010) Loss of heterozygosity tuberous sclerosis complex genes in multifocal micronodular pneumatocyte hyperplasia. Mod Pathol 23:1251–1260
Higashino T, Okazaki M, Mori H et al (2018) Microanatomy of sensory nerves in the upper eyelid: a cadaveric anatomical study. Plast Reconstr Surg 142:345–353
Hirano-Kawamoto A, Honkura Y, Shibata S et al (2015) Cricoarytenoid articulation in elderly Japanese with special reference to morphology of the synovial tissue. Ann Otol Rhinol Laryngol 125:219–227
Irfan S (2015) Minimal orbicularis myectomy: does it relieve spasms in benign essential blepharospasm? Am J Cosmet Surg 32:178–186
Jin ZW, Kim JH, Yamamoto M et al (2022) Fetal growth of the constrictor pharyngis superior with special reference to when and how it meets the buccinator: an embryological basis of considerable individual variations in the palatopharyngeal anatomy in adults. Surg Radiol Anat 44:559–571
Jin ZW, Umeki S, Takeuchi Y et al (2022) Inferior oblique muscle of the eye: its fetal development with special reference to understanding of the frequent variants in adults. Folia Morphol (Warsz) 81:442–450
Katori Y, Rodriguez-Vazquez JF, Kawase T et al (2011) Early fetal development of hard tissue pulleys for the human superior oblique and tensor veli palatini muscles. Ann Anat 193:127–133
Kawase T, Shibata S, Katori Y et al (2012) Elastic fiber-mediated enthesis in the human middle ear. J Anat 221:331–340
Kinoshita H, Umezawa T, Omine Y et al (2013) Distribution of elastic fibers in the head and neck: a histological study using late-stage human fetuses. Anat Cell Biol 46:39–48
Motohashi O, Suzuki M, Shida N et al (1995) Subarachnoid haemorrhage-induced proliferation of leptomeningeal cells and deposition of extracellular matrices in the arachnoid granulations and subarachnoid space. Acta Neurochir (Wien) 136:88–91
Munteanu O, Filipoiu FN, Cirstoiu MM et al (2022) A systematic approach of the intrauterine morphogenesis of the human palpebral apparatus. Organogenesis 18(1–9):e2066453
Osanai H, Abe S, Rodríguez-Vázquez JF et al (2011) Human orbital muscle: a new point of view from the fetal development of extraocular connective tissue. Investig Ophthalmol Vis Sci 52:1501–1506
Osanai H, Rodríguez-Vázquez JF, Abe H et al (2011) Fetal check ligament connected between the conjunctiva and the medial and lateral recti. Investig Ophthalmol Vis Sci 52:7175–7179
Park SY, Baek S, Lee H (2020) Characterization of the upper tarsal plate growth in children: implication in pediatric eyelid surgery. J Craniofac Surg 31:1474–1476
Petrikovsky BM, Kaplan G, Holsten N (2003) Eyelid movements in normal human fetuses. J Clin Ultrasound 31:299–301
Rodríguez-Vázquez JF, Iglesias-Moreno MC, Poch A et al (2022) Fetal development and growth of the fissula ante fenestram in the human ear. Anat Rec 305:424–435
Sato M, Cho KH, Yamamoto M et al (2020) Cavernous sinus and abducens nerve in human fetuses near term. Surg Radiol Anat 42:761–767
Sevel D (1988) A reappraisal of the development of the eyelids. Eye 2:123–129
Sun MT, Pham DT, O’Connor AJ et al (2015) The biomechanics of eyelid tarsal tissue. J Biomech 48:3455–3459
Takanashi Y, Shibata S, Katori Y et al (2013) Fetal development of the elastic fiber-mediated enthesis in the human middle ear. Ann Anat 195:441–448
Tawfik HA, Abdulhafez MH, Fouad YA et al (2016) Embryologic and fetal development of the human eyelid. Ophthal Plast Reconstr Surg 32:407–414
Woitek R, Kasprian G, Lindner C et al (2013) Fetal eye movements on magnetic resonance imaging. PLoS ONE 8–10:e77439
Funding
This study was supported by Wonkwang University in 2023.
Author information
Authors and Affiliations
Contributions
KC: planning; data acquisition; writing; KH: planning; data analysis; critical appraisal; JK: data acquisition; data analysis; GM: conceptualization; data acquisition; writing; JV: supervision; critical appraisal; HA: supervision; critical appraisal.
Corresponding author
Ethics declarations
Conflict of interest
Authors are required to disclose financial or non-financial interests that are directly or indirectly related to the work submitted for publication.
Ethical approval
This study was approved by the ethics committee of Complutense University (B08/374) and by the Akita University Ethics Committee (no. 1428).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cho, K.H., Homma, Ki., Kim, J.H. et al. Growth of muscles and nerves in the upper eyelid: a morphometrical and immunohistochemical study using term human fetuses. Surg Radiol Anat 46, 317–326 (2024). https://doi.org/10.1007/s00276-024-03308-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00276-024-03308-x