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Foetal Sonographic Anogenital Distance Is Longer in Polycystic Ovary Syndrome Mothers

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Foetal Sonographic Anogenital Distance Is Longer in Polycystic Ovary Syndrome Mothers Journal of Clinical Medicine Article Foetal Sonographic Anogenital Distance Is Longer in Polycystic Ovary Syndrome Mothers Sharon Perlman 1,2,* , Yoel Toledano 2,3, Zvi Kivilevitch 1, Nufar Halevy 1,2, Elena Rubin 1 and Yinon Gilboa 1,2 1 The Helen Schneider Women’s Hospital, Rabin Medical Centre, Ultrasound Unit, Zeev Jabotinsky Rd 39, Petah Tikva 49100, Israel; [email protected] (Z.K.); [email protected] (N.H.); [email protected] (E.R.); [email protected] (Y.G.) 2 Sackler School of Medicine, Tel-Aviv University, Tel-Aviv 69978, Israel; [email protected] 3 Endocrinology Clinic, The Helen Schneider Women’s Hospital, Rabin Medical Centre, Petach Tikva 49100, Israel * Correspondence: [email protected]; Tel.: +972-547-481097 Received: 10 August 2020; Accepted: 2 September 2020; Published: 4 September 2020 Abstract: Anogenital distance (AGD) is a biomarker for the prenatal hormonal environment. Androgen excess is a key element in polycystic ovary syndrome (PCOS). The aim of this study was to assess the sonographic foetal AGD in a population of PCOS mothers in comparison to the general population. Foetal AGD was measured prospectively by 2D ultrasound in PCOS mothers and compared to prenatal AGD nomograms. The results were interpreted regarding maternal and foetal characteristics. The mean sonographic foetal AGD centile measurement in PCOS mothers was significantly longer in comparison to the general population (86.04% 18.22; p < 0.001). Estimated ± foetal weight and birthweight were appropriate for gestational age and did not correlate with AGD. Sonographic foetal AGD was significantly longer in PCOS diabetic mothers and in those who conceived following assisted reproduction treatments when compared to the general population (p < 0.001). Our results support the role of AGD as a biomarker of the prenatal hormonal environment and provide evidence for the hyperandrogenic effect in PCOS pregnancies on foetal androgenic status and genitalia development. Keywords: ano-genital distance; polycystic ovary syndrome; androgen; prenatal ultrasound 1. Introduction The anogenital distance (AGD) is an established anthropometric androgen-dependent parameter for genital development in animals and humans and is approximately twice as long in males than in females [1–3]. Animal models suggest that AGD is determined in utero [4,5]. AGD at birth reflects prenatal exposure to androgens during the masculinization programming window [6]. Several animal studies have shown that the female reproductive tract is susceptible to virilization by exogenous androgens, resulting in a longer AGD, and that exposure of the male reproductive tract to anti-androgens will result in a shorter AGD [7–9]. In humans, the AGD is correlated with reproductive potential in men [10,11] and women [12], with congenital anomalies of the genitalia in boys [13–16] and exposure to anti-androgens (mainly phthalate) in male neonates [17–19]. However, there are little data regarding the effect of the androgen milieu in utero on human foetal AGD [20,21]. In recent years we have reported the feasibility of prenatal sonographic measurement of the AGD [22] and have established foetal AGD as a quantitative biomarker of androgen exposure during the critical embryonic window of genital development [23]. These findings were confirmed in a study published by Aydin et al. in 2019 [24]. Comparisons of foetal sonographic AGD measurements obtained by Israeli and British J. Clin. Med. 2020, 9, 2863; doi:10.3390/jcm9092863 www.mdpi.com/journal/jcm J. Clin. Med. 2020, 9, 2863 2 of 8 J. Clin. Med. 2020, 9, x FOR PEER REVIEW 2 of 8 obtainedcohorts revealed by Israeli significant and British di ffcohortserences, revealed and the si authorsgnificant recommended differences, and the the use authors of population-specific recommended thenormative use of population-specific values for accurate normative clinical assessments. values for accurate clinical assessments. Mothers withwith polycysticpolycystic ovary ovary syndrome syndrome (PCOS), (PCOS), the mostthe most common common endocrine endocrine disorder disorder in women in womenof reproductive of reproductive age, have age, higher have higher concentrations concentrations of circulating of circulating androgens androgens during during pregnancy pregnancy [25]. [25].Therefore, Therefore, this populationthis population can serve can serve to investigate to investigate the eff ectsthe effects of an androgenic of an androgenic environment environment during duringearly foetal early lifefoetal on life in-utero on in-utero development. development. In the In presentthe present study study we aimedwe aimed to exploreto explore the the eff ecteffect of ofmaternal maternal PCOS PCOS on on prenatal prenatal sonographic sonographic male male and and female female foetal foetal AGD. AGD. 2. Methods Methods A prospective pilot study was conducted over a period of 12 months. Inclusion criteria included a a well-dated pregnanc pregnancyy (last menstruation date or embryo transfer date confirmed confirmed by first-trimester first-trimester crown rump length) and absence of associated major anomalies, includingincluding anomaliesanomalies a ffaffectingecting the the genitalia genitalia such such as hypospadias, as hypospadias, the abdominal the abdominal wall and wall theperineum. and the perineum.PCOS was PCOS defined was according defined to according Rotterdam to criteria; Rotterdam i.e., thecriteria; presence i.e., ofthe two presence of the followingof two of three the followingcriteria: oligo-anovulation, three criteria: oligo-anovulation, hyperandrogenism hype/hyperandrogenaemiarandrogenism/hyperandrogenaemia and polycystic ovariesand polycystic seen at ovariesultrasound seen in at the ultrasound absence ofin allthe other absence endocrinopathies of all other endocrinopathies [26]. [26]. Sonographic examinations examinations were were performed performed with with an an E10 E10 expert expert machine (GE (GE Medical Medical Systems, Systems, Kretz Ultrasound, Zipf, Austria), equipped withwith an abdominal RAB6-D 2–8 MHz probe. The anogenital distance distance was was measured measured as as descr describedibed by by our our group group [22] [22] from from the the target target sign, sign, representing the foetal anus to the posterior base of the scrotum scrotum in males males or or the the posterior posterior commissure commissure of the labia in females (Figure 11).). Measurements werewere performedperformed byby experiencedexperienced obstetriciansobstetricians withwith aa sub-specialty inin prenatalprenatal imaging imaging (SP, (SP, YG). YG). For For each each foetus, foetus, measurements measurements were were performed performed three timesthree timesand the and mean the mean served served for statistical for statistical analyses. analyses Reproducibility. Reproducibility of measurements of measurements for sonographic for sonographic foetal foetalAGD (inter-AGD (inter- and intra-observer and intra-observer variability) variability) was assessedwas assessed in our inprevious our previous study study and and confirmed confirmed in a infollowing a following study, study, revealing revealing excellent excellent or substantial or substantial agreement agreement [22,24 [22,24].]. Figure 1. SonographicSonographic landmarks landmarks for for ano-genita ano-genitall distance distance measurement measurement in male in male (a) (anda) and female female (b) foetuses.(b) foetuses. In an In axial an axial view, view, at atthe the level level of ofthe the foet foetalal perineum, perineum, the the ano-genital ano-genital distance distance is is measured fromfrom the foetal anus to the base of the the scrotum scrotum in the the male male or or to to the the posterior posterior commissure commissure of the labia inin females. females. Gender-specificGender-specific centiles were calculated for the relevant gestational week according to local reference data [27]. [27]. Demographic data regarding maternal characteristics, obstetric results and neonatal outcome were retrieved from computerized medicalmedical charts.charts. Statistical analyses were performed with SPSS SPSS version version 22.0 22.0 software software (IBM (IBM Corporation, Corporation, Armonk, Armonk, NY, USA). Measurements of foetal sonographic anogenital distance were analysed referring to published local normative data [22]. Differences in regard to maternal and foetal characteristics were calculated by an independent t-test, comparing the mean for gestational age for each gender. J. Clin. Med. 2020, 9, 2863 3 of 8 J. Clin. Med. 2020, 9, x FOR PEER REVIEW 3 of 8 Measurements of foetal sonographic anogenital distance were analysed referring to published The Z-score was calculated referring to mean normal value per week of gestation and gender local normative data [22]. Differences in regard to maternal and foetal characteristics were calculated according to published local normative data: measured AGD PCOS–mean normal value per week of by an independent t-test, comparing the mean for gestational age for each gender. gestation and gender according to normative local data [22]/normal standard deviation for each The Z-score was calculated referring to mean normal value per week of gestation and gender gestational week and gender. according to published local normative data: measured AGD PCOS–mean normal value per week Data were compared to local foetal AGD nomograms, and the Z-score (measured AGD PCOS– of gestation and gender according to normative local data [22]/normal standard deviation for each
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