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Anatomical Aspects of the Development of the Sense of Taste in Humans

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Anatomical Aspects of the Development of the Sense of Taste in Humans Anatomical Aspects of the Development of the Sense of Taste in Humans Maryam Correa (nee Shahbake) BSc (Hons I) This thesis was submitted in fulfilment of the requirements for the degree of Doctor of Philosophy to University of Western Sydney, College of Health and Science, School of Natural Sciences. September 2016 Content Declaration VI Acknowledgements VII List of Figures VIII List of Tables XIV List of Abbreviations XV Abstract XVII Chapter 1: General Introduction 1 1.1 Anatomy of the Peripheral Gustatory System 4 1.1.1 The Tongue 4 1.1.2 Taste Papillae 5 1.1.2.1 Fungiform Papilla 5 1.1.2.2 Circumvallate Papillae 7 1.1.2.3 Foliate Papilla 7 1.1.2.4 Conical Papilla 8 1.1.2.5 Filiform Papillae 9 1.1.3 Taste Buds 9 1.1.3.1 Taste Bud Distribution 11 1.1.3.2 Taste Bud Innervation 12 1.2 Development of the Peripheral Gustatory System 14 1.2.1 Foetal and Neonatal Development 14 1.2.1.1 Animal Studies 14 1.2.1.2 Human Studies 17 1.2.2 Infant to Adult Development 19 1.2.2.1 Animal Studies 19 1.2.2.2 Human Studies 20 1.2.3 Adult to Elderly 21 1.3 Methods Used to Study Peripheral Gustatory Anatomy 23 1.3.1 Taste Papillae 23 1.3.1.1 Magnifying Glass 23 1.3.1.2 Light Microscopy 24 1.3.1.3 Video-microscopy 25 1.3.1.4 Cell Counters 28 1.3.1.5 Contact Endoscopy 29 1.3.1.6 Summary of Findings Using Different Methods 34 1.3.2 Taste Buds 35 1.3.2.1 Light Microscopy 35 1.3.2.2 Electron Microscopy (EM) and Scanning Electron Microscopy (SEM) 36 1.3.2.3 Video-microscopy 37 1.3.2.4 Summary of Findings Using Different Methods 38 1.4 Behavioural and Psychophysical Studies of the Development of the Gustatory System 40 I 1.4.1 Newborn to Infant 40 1.4.2 Adolescent to Adult 41 1.4.3 Gustatory Perception 41 1.5 Diseases and Taste Disorders 44 1.5.1 Taste and Common Diseases in Children 46 1.5.1.1 Cystic Fibrosis 46 1.5.1.2 Diabetes Mellitus 47 1.5.1.3 Otitis Media 47 1.5.1.4 Radiation Therapy 48 1.5.1.5 Renal Disease 49 1.6 Summary 50 1.7 Aims of Thesis 51 Chapter 2: Development of a Rapid Method for Counting Fungiform Papillae 52 2.1 Introduction 53 2.2 Aims 54 2.3 Methods 54 2.3.1 Participants 54 2.3.2 Equipment 55 2.3.2.1 Video-microscopy Configuration 55 2.3.2.2 Digital Camera Configuration 56 2.3.3 Experimental Procedure 56 2.3.3.1 Staining Procedure 57 2.3.3.2 Digital Camera Procedure 59 2.3.3.3 Video-microscopy Procedure 60 2.3.4 Image Capture Analysis 60 2.3.4.1 Digital Camera Image Capture 61 2.3.4.2 Video-microscopy Image Capture 62 2.3.5 Fungiform Papilla Identification 63 2.3.6 Statistical Analysis 64 2.4 Results 65 2.4.1 Fungiform Papilla Counts with the Digital Camera and Video- microscopy Methods 65 2.4.2 Comparison of Papillae Counts Obtained Using the Digital Camera and Video-microscopy Methods 65 2.4.3 Individual Subject Differences in Fungiform Papillae Counts Between the Two Methods 67 2.4.4 Summary of Findings 70 2.5 Discussion 71 Chapter 3: Quantification of Fungiform Papillae Density During Human Development 74 3.1 General Introduction 75 II 3.2 Aims 76 3.3 General Methods 77 3.3.1 Participants 77 3.3.2 Equipment and Experimental Procedure 77 3.3.2.1 Staining Procedure 78 Part I: Fungiform Papillae Density and Their Distribution Patterns in Children and Adults 80 3.4 Introduction 81 3.5 Aims 81 3.6 Methods 82 3.6.1 Image Analysis 82 3.6.2 Statistical Analysis 84 3.7 Results 85 3.7.1 Overall Variation of Fungiform Papillae Density Between Age Groups 85 3.7.2 Variation of Fungiform Papillae Density Per Cm Intervals Between Age Groups 86 3.7.2.1 Variation of Fungiform Papillae Density in the First Cm of the Anterior Tongue 86 3.7.2.2 Variation of Fungiform Papillae in the Second Cm of the Anterior Tongue 87 3.7.3 Distribution Patterns of Fungiform Papillae in Children and Adults 89 3.7.4 Summary of Findings 95 Part II: Predicting Fungiform Papillae Density 96 3.8 Introduction 97 3.9 Aims 97 3.10 Methods 97 3.10.1 Image Analysis 98 3.10.2 Statistical Analysis 99 3.11 Results 99 3.11.1 Predictor(s) of the Total Fungiform Papillae Count for All Age Groups 99 3.11.2 Summary of Findings 102 Part III: A Comparative Study of Fungiform Papillae Counts of the Anterior Tongue 103 3.12 Introduction 104 3.13 Aims 104 3.14 Methods 105 3.14.1 Image Analysis 105 3.14.2 Statistical Analysis 106 3.15 Results 107 III 3.15.1 Fungiform Papillae Density in Areas X and Y 107 3.15.2 Overall Analysis of Fungiform Papillae Density in Areas X and Y of All Age Groups 107 3.15.3 Summary of Findings 108 3.16 Discussion 109 Chapter 4: Development of a Non-Staining Method for Counting Fungiform Papillae 115 4.1 Introduction 116 4.2 Aims 117 4.3 Methods 117 4.3.1 Participants 117 4.3.2 Equipment 117 4.3.3 Experimental Procedure 118 4.3.3.1 Stage 1; Tongue Wet and No-stain 118 4.3.3.2 Stage 2; Tongue Dried and No-stain 119 4.3.3.3 Stage 3; Tongue Dried, Stained and Dried 119 4.3.4 Image Analysis 121 4.3.4.1 Stage 1 and 2 Analyses 121 4.3.4.2 Stage 3 Analysis 121 4.3.5 Statistical Analysis 122 4.4 Results 123 4.4.1 Description of Fungiform Papillae in Each of the Three Stages 123 4.4.2 Counts of Fungiform Papillae in the Common 0.28 cm2 Circle Area of the Three Stages 127 4.4.3 Summary of Findings 129 4.5 Discussion 130 Chapter 5: The Effect of Chronic Renal Failure on Fungiform Papillae Density in Children 132 5.1 Introduction 133 5.1.1 Renal Failure 133 5.1.2 Effect of Renal Failure on Taste Sensitivity 135 5.1.3 Effects of Renal Failure on Taste Bud Density 136 5.2 Aims 137 5.3 Methods 138 5.3.1 Participants 138 5.3.1.1 Classification of the Patients 138 5.3.2 Experimental Procedure 140 5.3.3 Statistical Analysis 143 5.4 Results 143 5.4.1 Statistical Analysis of Fungiform Papillae Density and eGFR in Control and Patient Groups 143 IV 5.4.2 Topographical Variation of Fungiform Papillae in Control and Patient Groups 145 5.4.3 Summary of Findings 150 5.5 Discussion 151 Chapter 6: General Discussion 153 References 161 Appendix A 189 Appendix B 191 Appendix C 203 Appendix D 205 Appendix E 207 V I hereby declare that this submission is my own work and, to the best of my knowledge, does not represent the view or work of others, except where duly acknowledge in the text. No part of this thesis has been submitted for a higher degree at another university or institution. This project was approved by the Human Research Ethics Committee, University of Western Sydney, (HEC02/188). __________________ Maryam Correa (nee Shahbake) VI Acknowledgements I would like to thank my supervisors, Dr Ian Hutchinson, Professor David Laing, and Dr. Tony Jinks for their support and encouragement. I am forever grateful for all their guidance throughout my studies and without them these studies would not have been possible. Thank you to Carolina Segovia, Fiona Wilkes and Jessica Armstrong for their assistance and motivation. Many thanks to my parents who have supported and encouraged me throughout my life. A special thanks to my wonderful husband Alejandro, for all his inspirations throughout my studies. Thank you for being the first volunteer, technical wizard and solving everything by clicking two buttons! Thank you to my amazing daughters Jasmine and Jacinta who have showed me anything is possible. Last but not least, thanks to all the subjects who participated in this study, specially, all the children from Sydney Children’s Hospital, without the participants this study would not have been possible. VII List of Figures Figure 1.1: The human tongue showing the regional location of different types of papillae (Goldstein 1989) 4 Figure 1.2: Drawings of regions containing different types of papillae (Miller 1995) 5 Figure 1.3: (A) Topographical view of a circumvallate papilla showing the papilla surrounded by a moat. (B) Sectional view of a circumvallate papilla showing the location of the taste buds (Gartner and Hiatt 2000) 7 Figure 1.4: Dorsal view of foliate papillae. Arrows indicating the position of taste buds (Gartner and Hiatt 2000) 8 Figure 1.5: (A) Topographical view of filiform papillae surrounding fungiform papillae. (B) Sectional view of filiform papilla (Gartner and Hiatt 2000) 9 Figure 1.6: Drawing of different gustatory papillae. Red arrows show the location of taste buds (Ballard 1997) 10 Figure 1.7: Basic structure of a taste bud (Mistretta 1991; Gartner and Hiatt 2000) 11 Figure 1.8: Anatomy of peripheral taste pathways, including the cranial nerves VII, IX and X (Finger and Silver 1991) 13 Figure 1.9: Embryonic rat tongue and fungiform papilla development.
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