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Impact of Age on Submucosal Nerve Measurements in Rectal Biopsies from Patients

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Impact of Age on Submucosal Nerve Measurements in Rectal Biopsies from Patients Impact of Age on Submucosal Nerve Measurements in Rectal Biopsies from Patients with Hirschsprung Disease THESIS Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Sarah Beach, B.S. Graduate Program in Anatomy The Ohio State University 2020 Thesis Committee Melissa Quinn, PhD, Academic Advisor Miriam Conces, MD, Research Advisor Christopher Pierson, MD, PhD James Cray, PhD Copyrighted by Sarah Beach 2020 2 Abstract Hypertrophic submucosal nerves, defined as ≥ 40 microns in diameter, are considered supportive of a diagnosis of Hirschsprung disease (HSCR), but the effect of age on nerve diameter has not been well-studied. We sought to characterize the distribution of nerve diameter in ganglionated rectal biopsies and the significance of hypertrophic submucosal nerves in the diagnosis of Hirschsprung disease based on age. Rectal biopsies were performed at Nationwide Children’s Hospital, Columbus, Ohio, for the evaluation of Hirschsprung disease. The biopsies from 2017-2018 were retrospectively collected and reviewed. Hirschsprung disease status was determined by the presence or absence of ganglion cells. The diameter of the largest submucosal nerve was measured and compared between age groups. Within the two-year period, 179 rectal biopsies with adequate submucosa were identified. Ganglion cells were present in 151 biopsies, and 28 aganglionic biopsies were diagnosed as Hirschsprung disease. Submucosal nerve diameter range was 17.5-101.5 microns in non-Hirschsprung disease biopsies (non-HSCR) and 14-98 microns in HSCR biopsies. Across all ages, hypertrophic submucosal nerves were significantly associated with Hirschsprung disease [HSCR = 25/28 (83%) vs non-HSCR = 59/151 (39.1%), p=<0.0001] and showed a sensitivity of 89.29% and specificity of 60.93%. Stratified by ii age, the submucosal nerve diameter remained statistically significant for HSCR in patients <1 year of age [HSCR = 22/24 (91.7%) vs. non-HSCR 19/91 (20.9%), p=<0.0001] with sensitivity of 91.67% and specificity of 79.12%. Hypertrophic submucosal nerves were not statistically significant in patients ≥ 1 year of age [HSCR = 3/4 (75%) vs. non- HSCR = 40/60 (66.7%), p=1] and showed reduced sensitivity (75%) and specificity (33.33%) for the diagnosis for HSCR. Based on a receiver operating characteristic curve, a nerve diameter of 45 microns demonstrates the greatest sensitivity (88%) and specificity (83%) for HSCR. The average submucosal nerve diameter in non-HSCR rectal biopsies increases with age. Hypertrophic submucosal nerves are significantly associated with HSCR in patients <1 year of age but may have limited utility for the diagnosis of HSCR in patients >1 year of age. However, our data includes very few patients with HSCR that are >1 year, and additional studies are needed to evaluate biopsies from older children. iii Dedication This document is dedicated to my friends and family. iv Acknowledgements Without the help of each of my committee members, I would not have been able to perform this research project for my master’s thesis. I would like to thank Dr. Miriam Conces for being a wonderful research coordinator and mentor. She set aside hours of her time in the past year to work on this project with me, from confirming every single nerve measurement to editing drafts of this document. She helped me learn so much about a disease I previously did not know much about, and she was always there to answer my questions. I would not have been able to conduct the research without her support and guidance. I would like to thank Dr. Chris Pierson for being genuinely interested in helping his students and setting them up for success in their future careers. Without his help, I would not have found my research project – one with a heavy emphasis on anatomy while still suiting my interests in gastroenterology. I would like to thank Dr. James Cray for reading draft after draft of this thesis paper and consistently giving me advice to improve. His experience in organizing and writing research papers has been very helpful. I would like to thank Dr. Melissa Quinn for being an outstanding anatomy professor and guiding me on the right path. She was also there to support me in finding a project for my thesis and always had an open door to discuss my options. v Vita 2014……………………………………………………………Notre Dame-Cathedral Latin, Chardon, Ohio 2018………………………………………………………….…B.S. Food and Nutrition Sciences, Ohio University 2018 to present…………………………………………..Graduate Student, Division of Anatomy, The Ohio State University Field of Study Major Field: Anatomy vi Table of Contents Abstract………………………………………………………………………………………………………………………ii Dedication………………………………………………………………………………………………………………….iv Acknowledgements…………………………………………………………………………………………………….v Vita…………………………………………………………………………………………………………………………….vi List of Tables …………………………………………………………………………………………………………..…ix List of Figures……………………………………………………………………………………………………………..x Chapter 1: Introduction………………………………………………………………………………………………1 1.1: Hirschsprung Disease……………………………………………………………………………….1 Pathogenesis……………………………………………………………………………………….2 Diagnosis…………………………………………………………………………………………….3 Treatment…………………………………………………………………………………………..8 Emerging Therapies……………………………………………………………………………10 Chapter 2: Anatomy of Hirschsprung Disease – Large Intestine…………………………………12 2.1: Normal Anatomy of the Large Intestine and Anal Canal …………………………12 Embryological Development of the Large Intestine and Anal Canal……12 Histology of the Large Intestine and Anal Canal…………………………………15 Gross Anatomy of the Large Intestine and Anal Canal………………………..19 Innervation of the Large Intestine and Anal Canal……………………………..21 vii 2.2: Abnormal Anatomy of the Large Intestine and Anal Canal in Hirschsprung Disease…………………………………………………………………………………………………...24 Chapter 3: Purpose of Study……………………………………………………………………………………..25 Chapter 4: Methods………………………………………………………………………………………………….27 4.1 Study approval and gathering of the cases.................................................27 4.2 Measuring the submucosal nerve diameters..............................................29 4.3 Comparing non-HSCR and HSCR nerve diameters across ages....................30 4.4 Determining an optimal nerve cutoff point supportive of HSCR.................31 Chapter 5: Results……………………………………………………………………………………………………..33 5.1 Distribution of nerve diameter in non-HSCR patients……………………………….33 5.2 Comparison between nerve diameters of non-HSCR and HSCR patients….35 5.3 Determining optimal cutoff of nerve diameter in HSCR patients………….….43 Chapter 6: Discussion………………………………………………………………………………………………..45 References………………………………………………………………………………………………………………..48 viii List of Tables Table 1. Number of non-HSCR and HSCR cases across ages……………………………………….34 Table 2. Non-HSCR average nerve diameter with standard deviation, maximum nerve diameter, and minimum nerve diameter for age groups.………………………………34 Table 3. HSCR average nerve diameter with standard deviation, maximum nerve diameter, and minimum nerve diameter for age groups.…………………………………………..36 Table 4. Average submucosal nerve diameters in micrometers for non-HSCR and HSCR patients across ages with standard deviations.………………………………………………37 Table 5. Hypertrophic nerves in non-HSCR and HSCR biopsies by age, sensitivities and specificities for HSCR, and p-values across all ages ………………………………………..40 Table 6. HSCR patients separated as the number of false negative and true positive cases across ages ……….…………………………………………………………………………………………..41 Table 7. Non-HSCR patients separated as the number of false negative and true positive cases across ages.……….………………………………………………………………………………….42 ix List of Figures Figure 1. Layers in a full-thickness rectal biopsy…………………………………………………………..6 Figure 2. Inclusion and exclusion criteria ……………………………………………………………………28 Figure 3. Average submucosal nerve diameter in non-HSCR patients ………………………..35 Figure 4. Comparison of average submucosal nerve diameters in HSCR and non-HSCR patients across ages ……………………………………………………………………………………….38 Figure 5. Comparison of submucosal nerve diameters in non-HSCR and HSCR patients...............................................................................................................39 Figure 6. Receiver operating characteristic curve...........................................................44 x Chapter 1: Introduction 1.1 Hirschsprung Disease Hirschsprung disease (HSCR) is characterized by a lack of ganglion cells in the submucosal and myenteric plexuses at variable lengths of the distal gastrointestinal tract. The length of the aganglionic segment in HSCR may vary from the distal one to two cm just proximal to the dentate line (ultrashort segment HSCR) to the entire large intestine (total colonic HSCR) (Szylberg and Marszalek, 2014). The most common type of HSCR, accounting for seventy-five to eighty percent of all cases, is rectosigmoid HSCR, in which parts of the rectum and sigmoid colon are aganglionic (Das and Mohanty, 2017). Long segment HSCR, accounting for ten to fifteen percent of HSCR cases, affects a greater length of the large intestine and extends from the sigmoid colon to the descending or transverse colon (Das and Mohanty, 2017). However, there is still a component of the large intestine that is ganglionic in long segment HSCR. The rarest form of HSCR is total colonic aganglionosis (TCA). TCA, present in five to seven percent of HSCR cases, is characterized by the absence of ganglion cells throughout the entire length of the large
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