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A Validated Protocol to Quantify Severity of Male Urogenital Feminization Using the MOUSE (Mouse Objective Urethral Severity Evaluation)

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A Validated Protocol to Quantify Severity of Male Urogenital Feminization Using the MOUSE (Mouse Objective Urethral Severity Evaluation) nature publishing group Articles Translational Investigation A validated protocol to quantify severity of male urogenital feminization using the MOUSE (Mouse objective urethral severity evaluation) Ciro M. Amato1 and Krista A. McCoy1 BACKGROUND: Congenital abnormalities vary in presen- Congenital abnormalities induced by altered genital mor- tation, yet studies using model organisms tend to focus on phogenesis are surprisingly common in humans. For example, occurrence rather than severity of the defect. Scoring severity hypospadias is the second most common birth defect in the of abnormalities in model systems allows explicit hypothesis United States, occurring in almost 1% of males. In Denmark testing during basic, translational, and reverse translational rates are as high as 4.6% (2). Hypospadias occurs when the studies. We developed and validated a protocol to quantify urethra is shortened and opens along the shaft of the penis, severity of male urogenital feminization (hypospadias) in the rather than at the distal tip. It has a complex etiology and broad mouse model. Hypospadias is one of the most common birth variation in its presentation (3). Hypospadias severity in new- defects in the world. borns varies from requiring no intervention, to necessitating METHODS: To induce genital feminization, pregnant mice complete sex reassignment surgery and vaginoplasty (4). were exposed to different concentrations of the antiandro- In fact, the Hypospadias Objective Penile Evaluation gen vinclozolin. Genitalia were photographed at gestational (H.O.P.E.) scoring system is used, in humans, to evaluate the age 18.5. A dichotomous scoring system to evaluate genital severity of several surgically correctable genitalia abnormali- feminization was developed, and validated against histologi- ties (5) and facilitates evaluation of both preoperative options cal measurements of urethral length. A training protocol was and postoperative outcomes. Determining the mechanisms developed for novice scorers, and criteria were defined to eval- driving the variation in genitalia abnormalities will advance uate precision and accuracy of scores. our understanding of why they are occurring in humans, and RESULTS: Vinclozolin induced variation in hypospadias sever- aid development of therapies to reduce their occurrence and ity. Severity scores were tightly correlated with histologically incidence. Such mechanistic studies are most efficiently con- determined urethral length and both techniques showed ducted in established model systems that exhibit similar devel- similar dose–response relationships. Novice observers were opment and responsiveness to environmental perturbations. trained to precisely and accurately score hypospadias severity. Mice are the accepted model for investigating urogenital devel- CONCLUSION: This standardized scoring system advances opment (6). As in humans, hypospadias severity varies in mice. the mouse as a model to study urogenital development, However, current techniques to evaluate severity of genital and will facilitate research on the mechanisms driving geni- feminization and hypospadias in the mouse require destruc- tal feminization in males, and aid translational hypospadias tive techniques such as histology (7) or resin casting (8), which research. allow measurement of urethral length (which is shorter with hypospadias), but limit the use of tissues for genetic, physi- ological, or developmental studies. orphological variation occurs because developmental Reproductive abnormalities in rodents increase in severity Mand molecular mechanisms driving morphogenesis dif- with mixtures of endocrine disrupting chemicals (9), and many fer across genotypes and environments (1). Many traits, how- studies suggest that the increase in incidence of hypospadias ever, are studied in a binary context: present or absent; normal in humans is related to fetal endocrine disrupting chemicals or abnormal. This framework limits our ability to build a com- exposure (10). Here we develop the Mouse Objective Urethral plete, and integrated understanding of the mechanisms driv- Severity Evaluation (M.O.U.S.E), as a standardized scoring sys- ing morphogenesis because developmental processes do not tem for the mouse that allows efficient and consistent compari- induce binary outcomes. The scoring system we develop and sons of hypospadias severity to facilitate mechanistic studies, validate provides a fine scale quantification of the severity of a and comparisons across genetic and environmental manipu- common genital birth defect so that the mechanisms driving lations. This scoring system is validated against urethral his- differences in genital morphogenesis can be studied. tology, the accepted endpoint used to evaluate hypospadias 1Department of Biology, East Carolina University, Greenville, North Carolina. Correspondence: Ciro M. Amato ([email protected]) Received 29 March 2016; accepted 9 June 2016; advance online publication 7 September 2016. doi:10.1038/pr.2016.157 880 Pediatric REsEarch Volume 80 | Number 6 | December 2016 Copyright © 2016 International Pediatric Research Foundation, Inc. Standardized penis abnormality score Articles severity (11). We go further to show that scores are negatively trained two novice scorers, with different educational experi- associated with anogenital distance (AGD), a well accepted ences, (a biology graduate student and a high school English marker of masculinization. We provide a training protocol teacher) to score genitalia. Each person was trained for only that includes guidelines for determining when observers can 10 min prior to scoring. Important landmarks were indicated, precisely and accurately score severity and show that scorers and the trainer discussed the process of scoring using prac- with different educational backgrounds can properly use the tice pictures, which were not included in the examination set training protocol. M.O.U.S.E. provides a single measurement (Figure 2 and Supplementary Methods online). through which multiple laboratories can exchange informa- Precision was evaluated in two ways. First, observers scored tion about how genetic manipulations or environmental treat- a single set of 24 sample photographs two times and a Pearson’s ments influence genital development. correlation was run to determine if the two scoring attempts were consistent. A correlation coefficient of r = 0.8 between the RESULTS two attempts was required to be considered precise. Second, a To develop M.O.U.S.E. as a standardized hypospadias sever- paired t-test was run on the two scoring attempts to ensure that ity scoring protocol, we needed to compare individuals with a the difference in scores did not significantly deviate from zero range of hypospadias severities. To induce hypospadias at dif- (so that attempts were not different from one another). It is pos- ferent severities, pregnant mouse dams (N = 3) were exposed sible for scorers to be consistent but score differently between to one of four doses of the androgen antagonist vinclozolin (0, scoring sessions (e.g., consistently scoring lower in the second 100, 125, 150 mg/kg) every day for 4 d during the critical period session). Quantifying precision in these two distinct ways is for genitalia development (gestational age (GA) 13.5–16.5) rigorous and necessary for standardized results. Accuracy was (12). Genitalia of each pup (GA 18.5) was photographed in a evaluated by comparing M.O.U.S.E scores to the histologi- standard position (see Supplementary Methods online), his- cally determined urethral length. To be considered accurate, tologically processed, and evaluated based on predetermined urethral length and severity score had to show a significant landmarks (Figure 1a,b). Genital length scaled with urethral negative relationship (urethral length decreases as severity length at the same rate across all individuals (χ2 = 40.598, P = increases) and have a R2 ≥ 0.95 (see Supplementary Methods 1.45e−07, slope (B1)= 0.3205). Across all treatments, males dis- online and http://thescholarship.ecu.edu/handle/10342/5650, played 33% larger urethral lengths (χ2 = 108.47, P = 2.2e−16) for more methodological detail, practice pictures and corre- than control (0 mg/kg vinclozolin) females. However, males sponding histological data). from vinclozolin-treated groups exhibited a saturating dose- If the observers failed any precision or accuracy test, they dependent shortening of urethral length (χ2 = 18.307, P = were retrained on new practice pictures and underwent 1.88e−05, Figure 1c) relative to control males. the scoring process a second time using new sample photo- Next, we created a dichotomous key with defined scor- graphs. Both the graduate student and high school teacher ing criteria that distinguished among: normal (0), abnormal required two training sessions and a total of 45 and 30 min (1), feminized (2), and severely feminized (3) penis structure, (respectively) across both scoring sessions to meet the crite- based on comparing overall genital morphology and location ria described below (Table 1), at which point both individu- of the urethral exit (Figure 2 and Supplementary Methods als were considered capable of scoring hypospadias severity in online). We used the dichotomous key to evaluate pictures of future experiments. To facilitate standardized severity scoring genitalia generated in the dose response study. Analogous to across laboratories, we have provided a protocol for taking urethral length, hypospadias severity using M.O.U.S.E scores
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