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Development of the Penis During the Human Fetal Period (13 to 36 Weeks After Conception)

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Development of the Penis During the Human Fetal Period (13 to 36 Weeks After Conception) Development of the Penis during the Human Fetal Period (13 to 36 Weeks after Conception) Carla B. M. Gallo, Waldemar S. Costa, Angelica Furriel, Ana L. Bastos and Francisco J. B. Sampaio* From the Urogenital Research Unit, State University of Rio de Janeiro, Rio de Janeiro, Brazil Purpose: We analyzed the development of the area of the penis and erectile Abbreviations structures (corpora cavernosa and corpus spongiosum) and the thickness of the and Acronyms tunica albuginea during the fetal period (13 to 36 weeks after conception) in ¼ MRI magnetic resonance humans to establish normative patterns of growth. imaging Materials and Methods: We studied 56 male human fetuses at 13 to 36 weeks WPC ¼ week post conception after conception. We used histochemical and morphometric techniques to analyze the parameters of total penile area, area of corpora cavernosa, area of Accepted for publication May 20, 2013. Study received institutional ethical commit- corpus spongiosum, and thickness of tunica albuginea in the dorsal and ventral tee approval. regions using ImageJ software (National Institutes of Health, Bethesda, Supported by grants from the National Maryland). Council of Scientific and Technological Develop- ment (CNPq-Brazil) and the Foundation for Results: Between 13 and 36 weeks after conception the area of the penis varies Research Support of Rio de Janeiro (FAPERJ). from 0.95 to 24.25 mm2. The area of the corpora cavernosa varies from 0.28 to * Correspondence: Urogenital Research Unit, 9.12 mm2, and the area of the corpus spongiosum varies from 0.14 to 3.99 mm2. State University of Rio de Janeiro, Av. 28 de Setembro, 87, Fundos, Vila Isabel, Rio de The thickness of the tunica albuginea varies from 0.029 to 0.296 mm in the dorsal Janeiro, Brazil 20551-030 (e-mail: sampaio.uerj@ region and from 0.014 to 0.113 mm in the ventral region of the corpora cavernosa. gmail.com). Conclusions: We found a strong correlation between the total penile area, corpora cavernosa and corpus spongiosum with fetal age (weeks following conception). The growth rate was more intense during the second trimester (13 to 24 weeks of gestation) compared to the third trimester (25 to 36 weeks). Tunica albuginea thickness also was strongly correlated with fetal age and this struc- ture was thicker in the dorsal vs ventral region. Key Words: fetus, penis, growth ACCURATE data on genital develop- morphometric analysis of images ment in humans, especially the penis, such as ultrasound and MRI can are relatively scarce.1e6 Although the be complemented with macroscopic structural components of the penis and mesoscopic data that would present an important role in physi- characterize the growth of penile ology and pathology, there are few structures.8,9 studies on the development in In humans the growth of the penis human fetuses. occurs in 4 stages, ie in early preg- Ultrasonography for assessing the nancy, resulting in an average length external genitalia in utero has been of 3.5 cm in newborns; from birth to 2 used as a tool not only to determine years, when an increase of 1.5 cm is fetal gender, but also to characterize observed; from 2 to 11 years, with an the patterns of normal development.7 additional 1.5 cm growth, and at pu- The different patterns obtained by berty, when the penis reaches adult 0022-5347/13/1905-1876/0 http://dx.doi.org/10.1016/j.juro.2013.05.050 THE JOURNAL OF UROLOGY® Vol. 190, 1876-1883, November 2013 1876 j www.jurology.com © 2013 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION AND RESEARCH,INC. Printed in U.S.A. PENILE DEVELOPMENT IN HUMAN FETUSES 1877 size.10 The mechanism of growth cessation is still died of causes unrelated to the urogenital tract. The not completely clear.11 fetuses were well preserved and none had any detectable The development of the penis begins at 8 weeks of congenital malformation. Gestational age ranged from 13 gestation. Complete development of the urethra oc- to 36 weeks following conception (corresponding to 15 to curs in the 14th week of pregnancy and the foreskin 38 menstrual weeks) and was estimated by the greatest foot length method.19e22 The fetuses were dissected with a encircles the glans at 21 weeks.6,12,13 The length of magnification glass, and the urogenital bloc containing the penis increases significantly with fetal gesta- kidneys, ureters, bladder, prostate, testes and penis was tional age, from a value of approximately 6.0 mm at removed. We used 1 to 5 fetuses of each gestational age 14,15 16 weeks to 26.4 mm at 38 weeks. Although there (see table). have been studies on penile growth in the fetal period, they are related only to the length of the penis Tissue Sample Preparation based on ultrasound.9,14,16e18 To our knowledge there After dissection the penis was incised close to the pubic are no studies available on the growth of the penile symphysis, around 2 mm from it, cross-sectioned at its area during the fetal period. Our analysis started mid shaft and immediately immersed in 10% formalin during the fetal period, from 13 WPCs, which corre- phosphate buffer solution for 24 hours. Afterward the m sponds to 15 gestational (menstrual) weeks, when samples were embedded in paraffin and sectioned at 5 m with intervals of 200 mm between each section. The sam- the main elements of the penis, such as the corpora ples for histological analysis were obtained from the mid cavernosa, corpus spongiosum and tunica albuginea, shaft of the penis (fig. 1). The sections were stained with are already formed, as evidenced by our data. Masson trichrome for analysis and evaluation of the area We analyzed the growth of the area of the penis of the penis, corpora cavernosa and corpus spongiosum, and erectile structures (corpora cavernosa and and with hematoxylin and eosin for analysis of the tunica corpus spongiosum) and thickness of the tunica albuginea thickness. albuginea during the fetal period (13 to 36 weeks after conception), establishing normative patterns Morphometric Analysis of growth. Precise data on penile area growth dur- All sections were photographed with a digital camera ing the fetal period would be useful for correlation (DP70, Olympus America, Inc., Melville, New York) under  with clinical data obtained by ultrasound and the same conditions at a resolution of 2,040 1,536 pixels, directly coupled to the microscope (BX51, Olympus mainly by MRI, which can evaluate the sectional America, Inc.) and stored in a TIFF file. The ImageJ area in vivo. Tracking these data would also be software, version 1.46r, loaded with its own plug-in useful for evaluating and following cases of micro- (http://rsb.info.nih.gov/ij/) was used for penile evaluation penis in utero. (fig. 1). We obtained 5 sections from each penis. We analyzed 1 field on each section and we obtained 3 measurements for MATERIALS AND METHODS each field, considering the deep fascia of the penis (Buck The study protocol was approved by the ethical committee fascia) as the external limit (fig. 1, A). We then obtained on human research at our institution. We studied 56 the mean of these 3 measurements, determining the area penises from fresh normal human fetuses. All fetuses had of the penis. Area of penis, corpora cavernosa and corpus spongiosum, and thickness of tunica albuginea by WPC Mean mm2 Area Mean mm2 Area Mean mm Thickness of Mean mm Thickness of Mean mm2 Area of Penis of Corpora of Corpus Tunica Albuginea in the Tunica Albuginea in WPC No. Fetuses (range) Cavernosa (range) Spongiosum (range) Dorsal Region (range) Ventral Region (range) 13 1 0.956 (0.956e0.956) 0.280 (0.280e0.280) 0.140 (0.140e0.140) 0.029 (0.025e0.058) 0.014 (0.013e0.021) 14 5 1.733 (1.414e1.812) 0.393 (0.277e0.531) 0.268 (0.231e0.458) 0.031 (0.024e0.053) 0.021 (0.010e0.025) 15 4 1.470 (1.383e1.557) 0.492 (0.415e0.569) 0.264 (0.202e0.295) 0.041 (0.034e0.048) 0.025 (0.012e0.030) 16 2 3.969 (2.506e5.431) 1.202 (0.913e1.492) 0.624 (0.509e0.738) 0.054 (0.045e0.066) 0.028 (0.020e0.031) 17 4 3.780 (2.934e5.088) 1.642 (1.404e1.936) 0.636 (0.569e0.742) 0.049 (0.045e0.059) 0.038 (0.026e0.044) 18 5 4.607 (4.087e5.127) 1.425 (1.228e1.622) 0.892 (0.808e0.981) 0.043 (0.039e0.061) 0.031 (0.016e0.038) 20 5 10.350 (9.260e10.864) 2.716 (2.534e2.915) 1.019 (0.976e1.784) 0.074 (0.071e0.077) 0.021 (0.021e0.022) 21 4 11.791 (8.304e11.232) 4.903 (3.231e5.371) 1.915 (1.825e2.546) 0.107 (0.106e0.108) 0.073 (0.056e0.083) 22 4 9.727 (9.260e11.731) 3.260 (2.546e4.095) 1.441 (1.245e1.867) 0.171 (0.143e0.219) 0.062 (0.052e0.109) 23 3 10.894 (9.396e12.392) 2.672 (2.654e2.724) 1.435 (1.203e1.668) 0.103 (0.098e0.114) 0.065 (0.049e0.067) 24 4 11.232 (8.290e14.174) 3.050 (1.867e4.233) 1.847 (1.142e2.552) 0.194 (0.164e0.227) 0.084 (0.050e0.109) 25 4 11.731 (10.192e15.158) 4.869 (3.364e5.371) 1.894 (1.207e2.581) 0.156 (0.144e0.168) 0.097 (0.078e0.117) 27 4 17.513 (16.288e18.938) 8.678 (8.348e9.007) 3.469 (3.213e3.725) 0.190 (0.168e0.220) 0.119 (0.092e0.129) 28 1 21.104 (21.104e21.104) 9.866 (9.866e9.866) 3.717 (3.717e3.717) 0.329 (0.300e0.347) 0.134 (0.102e0.144) 29 2 18.956 (13.279e24.633) 5.450 (4.095e6.805) 3.031 (2.482e3.580) 0.174 (0.116e0.206) 0.115 (0.088e0.125) 30 1 19.319 (19.319e19.319) 5.817 (5.817e5.817) 2.578 (2.578e2.578) 0.271 (0.213e0.288) 0.094 (0.084e0.134) 32 1 16.692 (16.692e16.692) 5.013 (5.013e5.013) 3.175 (3.175e3.175) 0.266 (0.236e0.314) 0.096 (0.075e0.108) 33 1 20.770 (20.770e20.770) 8.832 (8.832e8.832) 3.243 (3.243e3.243) 0.293 (0.252e0.319) 0.138 (0.099e0.143) 36 1 24.250 (24.250e24.250) 9.120 (9.120e9.120) 3.990 (3.990e3.990) 0.296 (0.226e0.338) 0.113 (0.098e0.153) 1878 PENILE DEVELOPMENT IN HUMAN FETUSES Figure 1.
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