Talk:Hearing - Middle Ear Development: Difference between revisions

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© 2011 The Authors. Journal of Anatomy © 2011 Anatomical Society of Great Britain and Ireland.
© 2011 The Authors. Journal of Anatomy © 2011 Anatomical Society of Great Britain and Ireland.


PMID: 21477146
PMID 21477146


===Can you hear me now? Understanding vertebrate middle ear development===
===Can you hear me now? Understanding vertebrate middle ear development===
Line 28: Line 28:
The middle ear is a composite organ formed from all three germ layers and the neural crest. It provides the link between the outside world and the inner ear, where sound is transduced and routed to the brain for processing. Extensive classical and modern studies have described the complex morphology and origin of the middle ear. Non-mammalian vertebrates have a single ossicle, the columella. Mammals have three functionally equivalent ossicles, designated the malleus, incus and stapes. In this review, I focus on the role of genes known to function in the middle ear. Genetic studies are beginning to unravel the induction and patterning of the multiple middle ear elements including the tympanum, skeletal elements, the air-filled cavity, and the insertion point into the inner ear oval window. Future studies that elucidate the integrated spatio-temporal signaling mechanisms required to pattern the middle ear organ system are needed. The longer-term translational benefits of understanding normal and abnormal ear development will have a direct impact on human health outcomes.
The middle ear is a composite organ formed from all three germ layers and the neural crest. It provides the link between the outside world and the inner ear, where sound is transduced and routed to the brain for processing. Extensive classical and modern studies have described the complex morphology and origin of the middle ear. Non-mammalian vertebrates have a single ossicle, the columella. Mammals have three functionally equivalent ossicles, designated the malleus, incus and stapes. In this review, I focus on the role of genes known to function in the middle ear. Genetic studies are beginning to unravel the induction and patterning of the multiple middle ear elements including the tympanum, skeletal elements, the air-filled cavity, and the insertion point into the inner ear oval window. Future studies that elucidate the integrated spatio-temporal signaling mechanisms required to pattern the middle ear organ system are needed. The longer-term translational benefits of understanding normal and abnormal ear development will have a direct impact on human health outcomes.


PMID: 21196256
PMID 21196256


http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3065862
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3065862
Line 47: Line 47:
Copyright © 2010 Elsevier Ireland Ltd. All rights reserved.
Copyright © 2010 Elsevier Ireland Ltd. All rights reserved.


PMID: 21145599
PMID 21145599


==2010==
==2010==
Line 77: Line 77:
(c) 2009 Wiley-Liss, Inc.
(c) 2009 Wiley-Liss, Inc.


PMID: 19899117
PMID 19899117


===Defects in middle ear cavitation cause conductive hearing loss in the Tcof1 mutant mouse===
===Defects in middle ear cavitation cause conductive hearing loss in the Tcof1 mutant mouse===
Line 90: Line 90:
Conductive hearing loss (CHL) is one of the most common forms of human deafness. Despite this observation, a surprising gap in our understanding of the mechanisms underlying CHL remains, particularly with respect to the molecular mechanisms underlying middle ear development and disease. Treacher Collins syndrome (TCS) is an autosomal dominant disorder of facial development that results from mutations in the gene TCOF1. CHL is a common feature of TCS but the causes of the hearing defect have not been studied. In this study, we have utilized Tcof1 mutant mice to dissect the developmental mechanisms underlying CHL. Our results demonstrate that effective cavitation of the middle ear is intimately linked to growth of the auditory bulla, the neural crest cell-derived structure that encapsulates all middle ear components, and that defects in these processes have a profoundly detrimental effect on hearing. This research provides important insights into a poorly characterized cause of human deafness, and provides the first mouse model for the study of middle ear cavity defects, while also being of direct relevance to a human genetic disorder.
Conductive hearing loss (CHL) is one of the most common forms of human deafness. Despite this observation, a surprising gap in our understanding of the mechanisms underlying CHL remains, particularly with respect to the molecular mechanisms underlying middle ear development and disease. Treacher Collins syndrome (TCS) is an autosomal dominant disorder of facial development that results from mutations in the gene TCOF1. CHL is a common feature of TCS but the causes of the hearing defect have not been studied. In this study, we have utilized Tcof1 mutant mice to dissect the developmental mechanisms underlying CHL. Our results demonstrate that effective cavitation of the middle ear is intimately linked to growth of the auditory bulla, the neural crest cell-derived structure that encapsulates all middle ear components, and that defects in these processes have a profoundly detrimental effect on hearing. This research provides important insights into a poorly characterized cause of human deafness, and provides the first mouse model for the study of middle ear cavity defects, while also being of direct relevance to a human genetic disorder.


PMID: 20106873  
PMID 20106873  
http://www.ncbi.nlm.nih.gov/pubmed/20106873
http://www.ncbi.nlm.nih.gov/pubmed/20106873


Line 97: Line 97:
Amin S, Matalova E, Simpson C, Yoshida H, Tucker AS.
Amin S, Matalova E, Simpson C, Yoshida H, Tucker AS.
BMC Dev Biol. 2007 Dec 5;7:134.
BMC Dev Biol. 2007 Dec 5;7:134.
PMID: 18053235  
 
PMID 18053235  


"The malleus and incus first appear as a single united condensation expressing early cartilage markers. The incudomalleal joint region forms by cells in the presumptive joint region switching off cartilage markers and turning on joint markers. Failure in this process may result in fusion of this joint, as observed in human syndromes such as Branchio-Oto-Renal Syndrome or Treacher Collins Syndrome."
"The malleus and incus first appear as a single united condensation expressing early cartilage markers. The incudomalleal joint region forms by cells in the presumptive joint region switching off cartilage markers and turning on joint markers. Failure in this process may result in fusion of this joint, as observed in human syndromes such as Branchio-Oto-Renal Syndrome or Treacher Collins Syndrome."
Line 109: Line 110:
Abstract
Abstract
The dimensions and the mass of the auditive ossicles was determined bilaterally in 100 human fetuses, of each sex aged from 21 to 40 weeks and 20 individual adults aged 18 to 40 years. It was found that the development of auditive ossicles in human is not completed during fetal life. The analyzed parameters of malleus (a, b, c, d1, d2, e) in the over fetal life period increased adequately by 14.02%, 11.22%, 16.70%, 12.80%, 12.01%, 21.98%, incus by (a, b, c1, c2, d, e) - 7.61%, 11.48%, 11.40%, 23.59%, 12.14%, 14.94%, stapes by (a, b, c, d, e, f) - 6.28%, 7.66%, 8.40%, 4.54%, 4.54%, 4.16%. In the over fetal life period increase of weight of malleus by 22.05%, incus by 26.49%, stapes by 11.57% was also observed. Described parameters of ossicles system are very important with respect to classification to the operations improving hearing in the system convecting of vibration of the tympanic membrane in children.
The dimensions and the mass of the auditive ossicles was determined bilaterally in 100 human fetuses, of each sex aged from 21 to 40 weeks and 20 individual adults aged 18 to 40 years. It was found that the development of auditive ossicles in human is not completed during fetal life. The analyzed parameters of malleus (a, b, c, d1, d2, e) in the over fetal life period increased adequately by 14.02%, 11.22%, 16.70%, 12.80%, 12.01%, 21.98%, incus by (a, b, c1, c2, d, e) - 7.61%, 11.48%, 11.40%, 23.59%, 12.14%, 14.94%, stapes by (a, b, c, d, e, f) - 6.28%, 7.66%, 8.40%, 4.54%, 4.54%, 4.16%. In the over fetal life period increase of weight of malleus by 22.05%, incus by 26.49%, stapes by 11.57% was also observed. Described parameters of ossicles system are very important with respect to classification to the operations improving hearing in the system convecting of vibration of the tympanic membrane in children.
PMID: 2268059 [PubMed - indexed for MEDLINE]
 
PMID 2268059


==2005==
==2005==
Line 123: Line 125:
The objective of this study was to clarify the development of the stapes in humans and its relationship with the cartilage of the second branchial arch. The study was carried out in 25 human embryos between 6 and 28 mm crown-rump length. The stapes develops at the cranial end of the second branchial arch through an independent anlage of the cartilage of this arch. Between the stapedial anlage and the cranial end of the Reichert's cartilage there is a formation called the interhyale, the internal segment of which gives rise to the tendon of the stapedial muscle. The stapedial anlage is a unique formation with two distinct parts: the superior part that will comprise the base and the inferior part that will be crossed by the stapedial artery during embryonic development and will constitute the limbs and the head of the stapes. According to the results, the otic capsule is not involved in formation of the base of the stapes.
The objective of this study was to clarify the development of the stapes in humans and its relationship with the cartilage of the second branchial arch. The study was carried out in 25 human embryos between 6 and 28 mm crown-rump length. The stapes develops at the cranial end of the second branchial arch through an independent anlage of the cartilage of this arch. Between the stapedial anlage and the cranial end of the Reichert's cartilage there is a formation called the interhyale, the internal segment of which gives rise to the tendon of the stapedial muscle. The stapedial anlage is a unique formation with two distinct parts: the superior part that will comprise the base and the inferior part that will be crossed by the stapedial artery during embryonic development and will constitute the limbs and the head of the stapes. According to the results, the otic capsule is not involved in formation of the base of the stapes.


PMID: 16050903
PMID 16050903




Line 140: Line 142:
A microanalytical study of human auditory ossicles was performed in 11 normal adults, 13 infants, 13 foetuses, 7 middle ear cholesteatoma, 7 chronic otitis and 1 facial nerve schwannoma. Malleus and incus ossification is initiated in the foetal period, the Ca/P ratio reaching a value of 1.8-1.9 in the 29-gestation-week foetus and continues in the infant period until adult, except for the marginal area of the malleus head which appears mineralized in the infant. The normal Ca/P ratio for malleus is 2.10, and 2.19 for incus. In the stapes, mature Ca/P ratio values (2.11) appear in the footplate of the 23-gestation-weeks foetus. Stapes ossification continues in its head and crura, but never reaches malleus and incus values. We have confirmed that there is a relationship between Ca/P ratio and sulphur values in the ossification process; so when the first increases the second decreases. Finally, in our pathological material we have not found any significant alteration of Ca/P ratio, sulphur or other elements studied.
A microanalytical study of human auditory ossicles was performed in 11 normal adults, 13 infants, 13 foetuses, 7 middle ear cholesteatoma, 7 chronic otitis and 1 facial nerve schwannoma. Malleus and incus ossification is initiated in the foetal period, the Ca/P ratio reaching a value of 1.8-1.9 in the 29-gestation-week foetus and continues in the infant period until adult, except for the marginal area of the malleus head which appears mineralized in the infant. The normal Ca/P ratio for malleus is 2.10, and 2.19 for incus. In the stapes, mature Ca/P ratio values (2.11) appear in the footplate of the 23-gestation-weeks foetus. Stapes ossification continues in its head and crura, but never reaches malleus and incus values. We have confirmed that there is a relationship between Ca/P ratio and sulphur values in the ossification process; so when the first increases the second decreases. Finally, in our pathological material we have not found any significant alteration of Ca/P ratio, sulphur or other elements studied.


PMID: 1604999
PMID 1604999
http://www.ncbi.nlm.nih.gov/pubmed/1604999

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Cite this page: Hill, M.A. (2024, March 28) Embryology Hearing - Middle Ear Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Talk:Hearing_-_Middle_Ear_Development

guinea pig the malleus and incus are normally found as a single complex

2011

Closure of the middle ear with special reference to the development of the tegmen tympani of the temporal bone

J Anat. 2011 Apr 8. doi: 10.1111/j.1469-7580.2011.01378.x. [Epub ahead of print]

Rodríguez-Vázquez JF, Murakami G, Verdugo-López S, Abe SI, Fujimiya M. Department of Anatomy and Human Embryology II, Faculty of Medicine, Embryology Institute, University Complutense of Madrid, Spain Division of Internal Medicine, Iwamizawa Kojin-kai Hospital, Iwamizawa, Japan Oral Health Science Center HRC7, Tokyo Dental College, Chiba-City, Chiba, Japan Department of Anatomy, Sapporo Medical University School of Medicine, Sapporo, Japan.

Abstract Closure of the middle ear is believed to be closely related to the evolutionary development of the mammalian jaw. However, few comprehensive descriptions are available on fetal development. We examined paraffin-embedded specimens of 20 mid-term human fetuses at 8-25 weeks of ovulation age (crown-rump length or CRL, 38-220 mm). After 9 weeks, the tympanic bone and the squamous part of the temporal bone, each of which was cranial or caudal to Meckel's cartilage, grew to close the lateral part of the tympanosquamosal fissure. At the same time, the cartilaginous tegmen tympani appeared independently of the petrous part of the temporal bone and resulted in the petrosquamosal fissure. Subsequently, the medial part of the tympanosquamosal fissure was closed by the descent of a cartilaginous inferior process of the tegmen tympani. When Meckel's cartilage changed into the sphenomandibular ligament and the anterior ligament of the malleus, the inferior process of the tegmen tympani interposed between the tympanic bone and the squamous part of the temporal bone, forming the petrotympanic fissure for the chorda tympani nerve and the discomalleolar ligament. Therefore, we hypothesize that, in accordance with the regression of Meckel's cartilage, the rapidly growing temporomandibular joint provided mechanical stress that accelerated the growth and descent of the inferior process of the tegmen tympani via the discomalleolar ligament. The usual diagram showing bony fissures around the tegmen tympani may overestimate the role of the tympanic bone in the fetal middle-ear closure. © 2011 The Authors. Journal of Anatomy © 2011 Anatomical Society of Great Britain and Ireland.

PMID 21477146

Can you hear me now? Understanding vertebrate middle ear development

Front Biosci. 2011 Jan 1;16:1675-92.

Chapman SC. Clemson University, Biological Sciences, 132 Long Hall, Clemson, SC 29634, USA. schapm2@clemson.edu

Abstract

The middle ear is a composite organ formed from all three germ layers and the neural crest. It provides the link between the outside world and the inner ear, where sound is transduced and routed to the brain for processing. Extensive classical and modern studies have described the complex morphology and origin of the middle ear. Non-mammalian vertebrates have a single ossicle, the columella. Mammals have three functionally equivalent ossicles, designated the malleus, incus and stapes. In this review, I focus on the role of genes known to function in the middle ear. Genetic studies are beginning to unravel the induction and patterning of the multiple middle ear elements including the tympanum, skeletal elements, the air-filled cavity, and the insertion point into the inner ear oval window. Future studies that elucidate the integrated spatio-temporal signaling mechanisms required to pattern the middle ear organ system are needed. The longer-term translational benefits of understanding normal and abnormal ear development will have a direct impact on human health outcomes.

PMID 21196256

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3065862

Development of the stapedius muscle canal and its possible clinical consequences

Int J Pediatr Otorhinolaryngol. 2011 Feb;75(2):277-81. Epub 2010 Dec 10.

Cisneros A, Orozco JR, Nogues JA, Gotor CY, Orozco AW, de la Torre MA, Gil AV. Department of Human Anatomy and Histology, School of Medicine, University of Zaragoza, C/ Domingo Miral, s/n, 50009 Zaragoza, Spain. aicisner@unizar.es

Abstract

OBJECTIVE: To study the development of the stapedius muscle canal in human embryos and foetuses. MATERIALS AND METHODS: 46 temporal bones with ages between 9mm and new-borns were studied. The preparations were dyed using Martins' trichrome technique. RESULTS: Two areas of different embryological origin form the stapedius muscle canal, which contains this muscle and the facial nerve. On the otic capsule, at 11 weeks an extension starts to grow from its caudal part, which moves outwards and near to Reichert's cartilage, forming the footplate and internal wall. The pyramidal eminence comes from the mesenchyme that surrounds the muscle, forming a partition to separate it from the laterohyale portion of Reichert's cartilage. Extensive connections are observed in its development between bone marrow and mesenchyme. At 35 weeks the muscle and nerve start to separate by means of a bony partition. If this partition does not form, there is going to be a dehiscence that could cause peripheral nerve pathology due to the repeated contraction of the muscle, or the dissemination of infections from middle ear. CONCLUSION: During the development of the stapedius muscle canal the presence of dehiscences between the facial nerve and the muscle may have clinical repercussions.

Copyright © 2010 Elsevier Ireland Ltd. All rights reserved.

PMID 21145599

2010

History of studies on mammalian middle ear evolution: a comparative morphological and developmental biology perspective

J Exp Zool B Mol Dev Evol. 2010 Sep 15;314(6):417-33.

Takechi M, Kuratani S. Source Evolutionary Morphology Research Group, Center for Developmental Biology, RIKEN, Kobe,Hyogo, Japan. sabaidee@cdb.riken.jp

Abstract

The mammalian middle ear represents one of the most fundamental morphological features that define this class of vertebrates. Its skeletal pattern differs conspicuously from those of other amniotes and has attracted the attention of comparative zoologists for about 200 years. To reconcile this morphological inconsistency, early comparative morphologists suggested that the mammalian middle ear was derived from elements of the jaw joint of nonmammalian amniotes. Fossils of mammalian ancestors also implied a transition in skeletal morphology that resulted in the mammalian state. During the latter half of the 20th century, developmental mechanisms controlling the formation of the jaw skeleton became the subject of studies in developmental biology and molecular genetics. Mammalian middle ear evolution can now be interpreted as a series of changes in the developmental program of the pharyngeal arches. In this review, we summarize the history of middle ear research, highlight some of the remaining problems, and suggest possible future directions. We propose that to understand mammalian middle ear evolution, it is essential to identify the critical developmental events underlying the particular mammalian anatomy and to describe the evolutionary sequence of changes in developmental and molecular terms. We also discuss the degree of consistency between the developmental explanation of the mammalian middle ear based on molecular biology and morphological changes in the fossil record.

(c) 2010 Wiley-Liss, Inc.

PMID 20700887


Development of the stapedius muscle and unilateral agenesia of the tendon of the stapedius muscle in a human fetus

Anat Rec (Hoboken). 2010 Jan;293(1):25-31.

Rodríguez-Vázquez JF, Mérida-Velasco JR, Verdugo-López S. Departamento de Anatomía y Embriología Humana II, Facultad de Medicina, Universidad Complutense, Madrid, España. jfrodvaz@med.ucm.es

Abstract

The objective was to analyze the development of the stapedius muscle to understand an isolated unilateral absence of the tendon of the stapedius muscle in a human fetus. The study was made on 50 human embryos and fetuses aged 38 days to 17 weeks post-conception. The stapedius muscle was formed by two anlagen, one for the tendon, which derives from the internal segment of the interhyale and another for the belly, located in the second pharyngeal arch, medially to the facial nerve and near the interhyale. In the interhyale, two segments were observed forming an angle and delimited by the attachment of the belly of the stapedius muscle. The internal segment will form the tendon. The lateral segment of the interhyale was attached to the cranial end of the Reichert's cartilage (laterohyale), and normally it disappears at the beginning of the fetal period. The right unilateral agenesia of the tendon of the stapedius muscle, observed for the first time in a human fetus of 14 weeks post-conception development (PCd), was brought about by the lack of formation or the regression of the internal segment of the interhyale. It presented a belly of the stapedius muscle with an anomalous arrangement, and with a pseudo tendon originated by the persistence of the external segment of the interhyale. (c) 2009 Wiley-Liss, Inc.

PMID 19899117

Defects in middle ear cavitation cause conductive hearing loss in the Tcof1 mutant mouse

Hum Mol Genet. 2010 Apr 15;19(8):1551-60. Epub 2010 Jan 27.

Richter CA, Amin S, Linden J, Dixon J, Dixon MJ, Tucker AS. Source Department of Craniofacial Development, Dental Institute, King's College London, London SE1 9RT, UK.

Abstract

Conductive hearing loss (CHL) is one of the most common forms of human deafness. Despite this observation, a surprising gap in our understanding of the mechanisms underlying CHL remains, particularly with respect to the molecular mechanisms underlying middle ear development and disease. Treacher Collins syndrome (TCS) is an autosomal dominant disorder of facial development that results from mutations in the gene TCOF1. CHL is a common feature of TCS but the causes of the hearing defect have not been studied. In this study, we have utilized Tcof1 mutant mice to dissect the developmental mechanisms underlying CHL. Our results demonstrate that effective cavitation of the middle ear is intimately linked to growth of the auditory bulla, the neural crest cell-derived structure that encapsulates all middle ear components, and that defects in these processes have a profoundly detrimental effect on hearing. This research provides important insights into a poorly characterized cause of human deafness, and provides the first mouse model for the study of middle ear cavity defects, while also being of direct relevance to a human genetic disorder.

PMID 20106873 http://www.ncbi.nlm.nih.gov/pubmed/20106873

2007

Incudomalleal joint formation: the roles of apoptosis, migration and downregulation

Amin S, Matalova E, Simpson C, Yoshida H, Tucker AS. BMC Dev Biol. 2007 Dec 5;7:134.

PMID 18053235

"The malleus and incus first appear as a single united condensation expressing early cartilage markers. The incudomalleal joint region forms by cells in the presumptive joint region switching off cartilage markers and turning on joint markers. Failure in this process may result in fusion of this joint, as observed in human syndromes such as Branchio-Oto-Renal Syndrome or Treacher Collins Syndrome."


Anat Anz. 1990;171(3):187-91. [The morphometry of the ear ossicles in humans during development] [Article in German] Olszewski J. Anstalt für Normale Anatomie, Medizinischen Militärakademie Lódź, Polen. Abstract The dimensions and the mass of the auditive ossicles was determined bilaterally in 100 human fetuses, of each sex aged from 21 to 40 weeks and 20 individual adults aged 18 to 40 years. It was found that the development of auditive ossicles in human is not completed during fetal life. The analyzed parameters of malleus (a, b, c, d1, d2, e) in the over fetal life period increased adequately by 14.02%, 11.22%, 16.70%, 12.80%, 12.01%, 21.98%, incus by (a, b, c1, c2, d, e) - 7.61%, 11.48%, 11.40%, 23.59%, 12.14%, 14.94%, stapes by (a, b, c, d, e, f) - 6.28%, 7.66%, 8.40%, 4.54%, 4.54%, 4.16%. In the over fetal life period increase of weight of malleus by 22.05%, incus by 26.49%, stapes by 11.57% was also observed. Described parameters of ossicles system are very important with respect to classification to the operations improving hearing in the system convecting of vibration of the tympanic membrane in children.

PMID 2268059

2005

Development of the stapes and associated structures in human embryos

J Anat. 2005 Aug;207(2):165-73.

Rodríguez-Vázquez JF. Departamento de Anatomía y Embriología Humana II, Facultad de Medicina, Universidad Complutense, Madrid, Spain. jfrodvaz@med.ucm.es

Abstract

The objective of this study was to clarify the development of the stapes in humans and its relationship with the cartilage of the second branchial arch. The study was carried out in 25 human embryos between 6 and 28 mm crown-rump length. The stapes develops at the cranial end of the second branchial arch through an independent anlage of the cartilage of this arch. Between the stapedial anlage and the cranial end of the Reichert's cartilage there is a formation called the interhyale, the internal segment of which gives rise to the tendon of the stapedial muscle. The stapedial anlage is a unique formation with two distinct parts: the superior part that will comprise the base and the inferior part that will be crossed by the stapedial artery during embryonic development and will constitute the limbs and the head of the stapes. According to the results, the otic capsule is not involved in formation of the base of the stapes.

PMID 16050903


http://onlinelibrary.wiley.com/doi/10.1111/j.1469-7580.2005.00441.x/full


A microanalytical study on human auditory ossicles in normal and pathological conditions

Acta Otolaryngol. 1992;112(2):317-21.

Sánchez-Fernández JM, Saint-Gerons S, Sánchez del Rey A. Source Department of Otolaryngology, School of Medicine, University of the Basque Country, Bilbao, Spain.

Abstract

A microanalytical study of human auditory ossicles was performed in 11 normal adults, 13 infants, 13 foetuses, 7 middle ear cholesteatoma, 7 chronic otitis and 1 facial nerve schwannoma. Malleus and incus ossification is initiated in the foetal period, the Ca/P ratio reaching a value of 1.8-1.9 in the 29-gestation-week foetus and continues in the infant period until adult, except for the marginal area of the malleus head which appears mineralized in the infant. The normal Ca/P ratio for malleus is 2.10, and 2.19 for incus. In the stapes, mature Ca/P ratio values (2.11) appear in the footplate of the 23-gestation-weeks foetus. Stapes ossification continues in its head and crura, but never reaches malleus and incus values. We have confirmed that there is a relationship between Ca/P ratio and sulphur values in the ossification process; so when the first increases the second decreases. Finally, in our pathological material we have not found any significant alteration of Ca/P ratio, sulphur or other elements studied.

PMID 1604999