A Synchrotron and Micro-CT Study of the Human Endolymphatic Duct System: Is Meniere's Disease Caused by an Acute Endolymph Backflow?

Background: The etiology of Meniere's disease (MD) and endolymphatic hydrops believed to underlie its symptoms remain unknown. One reason may be the exceptional complexity of the human inner ear, its vulnerability, and surrounding hard bone. The vestibular organ contains an endolymphatic duct s...

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Main Authors: Hao Li, Gunesh P. Rajan, Jeremy Shaw, Seyed Alireza Rohani, Hanif M. Ladak, Sumit Agrawal, Helge Rask-Andersen
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-05-01
Series:Frontiers in Surgery
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fsurg.2021.662530/full
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spelling doaj-7e7e93e0b8d44c67a146bbeca1d884842021-05-31T07:08:15ZengFrontiers Media S.A.Frontiers in Surgery2296-875X2021-05-01810.3389/fsurg.2021.662530662530A Synchrotron and Micro-CT Study of the Human Endolymphatic Duct System: Is Meniere's Disease Caused by an Acute Endolymph Backflow?Hao Li0Gunesh P. Rajan1Gunesh P. Rajan2Jeremy Shaw3Seyed Alireza Rohani4Hanif M. Ladak5Sumit Agrawal6Helge Rask-Andersen7Department of Surgical Sciences, Section of Otolaryngology and Head and Neck Surgery, Uppsala University Hospital, Uppsala, SwedenDepartment of Otolaryngology, Head and Neck Surgery, Luzerner Kantonsspital, Lucerne, SwitzerlandDepartment of Otolaryngology, Head and Neck Surgery Division of Surgery, Medical School, University of Western Australia, Perth, WA, AustraliaCentre for Microscopy, Characterisation and Analysis, Perth, WA, AustraliaDepartment of Otolaryngology-Head and Neck Surgery, Western University, London, ON, CanadaDepartment of Medical Biophysics and Department of Electrical and Computer Engineering, Western University, London, ON, CanadaDepartment of Otolaryngology-Head and Neck Surgery, Western University, London, ON, CanadaDepartment of Surgical Sciences, Section of Otolaryngology and Head and Neck Surgery, Uppsala University Hospital, Uppsala, SwedenBackground: The etiology of Meniere's disease (MD) and endolymphatic hydrops believed to underlie its symptoms remain unknown. One reason may be the exceptional complexity of the human inner ear, its vulnerability, and surrounding hard bone. The vestibular organ contains an endolymphatic duct system (EDS) bridging the different fluid reservoirs. It may be essential for monitoring hydraulic equilibrium, and a dysregulation may result in distension of the fluid spaces or endolymphatic hydrops.Material and Methods: We studied the EDS using high-resolution synchrotron phase contrast non-invasive imaging (SR-PCI), and micro-computed tomography (micro-CT). Ten fresh human temporal bones underwent SR-PCI. One bone underwent micro-CT after fixation and staining with Lugol's iodine solution (I2KI) to increase tissue resolution. Data were processed using volume-rendering software to create 3D reconstructions allowing orthogonal sectioning, cropping, and tissue segmentation.Results: Combined imaging techniques with segmentation and tissue modeling demonstrated the 3D anatomy of the human saccule, utricle, endolymphatic duct, and sac together with connecting pathways. The utricular duct (UD) and utriculo-endolymphatic valve (UEV or Bast's valve) were demonstrated three-dimensionally for the first time. The reunion duct was displayed with micro-CT. It may serve as a safety valve to maintain cochlear endolymph homeostasis under certain conditions.Discussion: The thin reunion duct seems to play a minor role in the exchange of endolymph between the cochlea and vestibule under normal conditions. The saccule wall appears highly flexible, which may explain occult hydrops occasionally preceding symptoms in MD on magnetic resonance imaging (MRI). The design of the UEV and connecting ducts suggests that there is a reciprocal exchange of fluid among the utricle, semicircular canals, and the EDS. Based on the anatomic framework and previous experimental data, we speculate that precipitous vestibular symptoms in MD arise from a sudden increase in endolymph pressure caused by an uncontrolled endolymphatic sac secretion. A rapid rise in UD pressure, mediated along the fairly wide UEV, may underlie the acute vertigo attack, refuting the rupture/K+-intoxication theory.https://www.frontiersin.org/articles/10.3389/fsurg.2021.662530/fullhumansynchrotron radiation phase-contrast imagingreunion ductBast's valveMeniere's disease
collection DOAJ
language English
format Article
sources DOAJ
author Hao Li
Gunesh P. Rajan
Gunesh P. Rajan
Jeremy Shaw
Seyed Alireza Rohani
Hanif M. Ladak
Sumit Agrawal
Helge Rask-Andersen
spellingShingle Hao Li
Gunesh P. Rajan
Gunesh P. Rajan
Jeremy Shaw
Seyed Alireza Rohani
Hanif M. Ladak
Sumit Agrawal
Helge Rask-Andersen
A Synchrotron and Micro-CT Study of the Human Endolymphatic Duct System: Is Meniere's Disease Caused by an Acute Endolymph Backflow?
Frontiers in Surgery
human
synchrotron radiation phase-contrast imaging
reunion duct
Bast's valve
Meniere's disease
author_facet Hao Li
Gunesh P. Rajan
Gunesh P. Rajan
Jeremy Shaw
Seyed Alireza Rohani
Hanif M. Ladak
Sumit Agrawal
Helge Rask-Andersen
author_sort Hao Li
title A Synchrotron and Micro-CT Study of the Human Endolymphatic Duct System: Is Meniere's Disease Caused by an Acute Endolymph Backflow?
title_short A Synchrotron and Micro-CT Study of the Human Endolymphatic Duct System: Is Meniere's Disease Caused by an Acute Endolymph Backflow?
title_full A Synchrotron and Micro-CT Study of the Human Endolymphatic Duct System: Is Meniere's Disease Caused by an Acute Endolymph Backflow?
title_fullStr A Synchrotron and Micro-CT Study of the Human Endolymphatic Duct System: Is Meniere's Disease Caused by an Acute Endolymph Backflow?
title_full_unstemmed A Synchrotron and Micro-CT Study of the Human Endolymphatic Duct System: Is Meniere's Disease Caused by an Acute Endolymph Backflow?
title_sort synchrotron and micro-ct study of the human endolymphatic duct system: is meniere's disease caused by an acute endolymph backflow?
publisher Frontiers Media S.A.
series Frontiers in Surgery
issn 2296-875X
publishDate 2021-05-01
description Background: The etiology of Meniere's disease (MD) and endolymphatic hydrops believed to underlie its symptoms remain unknown. One reason may be the exceptional complexity of the human inner ear, its vulnerability, and surrounding hard bone. The vestibular organ contains an endolymphatic duct system (EDS) bridging the different fluid reservoirs. It may be essential for monitoring hydraulic equilibrium, and a dysregulation may result in distension of the fluid spaces or endolymphatic hydrops.Material and Methods: We studied the EDS using high-resolution synchrotron phase contrast non-invasive imaging (SR-PCI), and micro-computed tomography (micro-CT). Ten fresh human temporal bones underwent SR-PCI. One bone underwent micro-CT after fixation and staining with Lugol's iodine solution (I2KI) to increase tissue resolution. Data were processed using volume-rendering software to create 3D reconstructions allowing orthogonal sectioning, cropping, and tissue segmentation.Results: Combined imaging techniques with segmentation and tissue modeling demonstrated the 3D anatomy of the human saccule, utricle, endolymphatic duct, and sac together with connecting pathways. The utricular duct (UD) and utriculo-endolymphatic valve (UEV or Bast's valve) were demonstrated three-dimensionally for the first time. The reunion duct was displayed with micro-CT. It may serve as a safety valve to maintain cochlear endolymph homeostasis under certain conditions.Discussion: The thin reunion duct seems to play a minor role in the exchange of endolymph between the cochlea and vestibule under normal conditions. The saccule wall appears highly flexible, which may explain occult hydrops occasionally preceding symptoms in MD on magnetic resonance imaging (MRI). The design of the UEV and connecting ducts suggests that there is a reciprocal exchange of fluid among the utricle, semicircular canals, and the EDS. Based on the anatomic framework and previous experimental data, we speculate that precipitous vestibular symptoms in MD arise from a sudden increase in endolymph pressure caused by an uncontrolled endolymphatic sac secretion. A rapid rise in UD pressure, mediated along the fairly wide UEV, may underlie the acute vertigo attack, refuting the rupture/K+-intoxication theory.
topic human
synchrotron radiation phase-contrast imaging
reunion duct
Bast's valve
Meniere's disease
url https://www.frontiersin.org/articles/10.3389/fsurg.2021.662530/full
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