Female genital malformations and their associated abnormalities
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1 Female genital and their associated abnormalities Peter Oppelt, M.D., a Meike von Have, M.D., a Mareike Paulsen, M.D., a Pamela L. Strissel, Ph.D., a Reiner Strick, Ph.D., a Sara Brucker, M.D., b Diethelm Wallwiener, M.D., b and Matthias W. Beckmann, M.D. a a Department of Gynecology and Obstetrics, University Hospital, Erlangen and b Department of Gynecology and Obstetrics, University Hospital, Tübingen, Germany Objective: With an incidence of up to 5% in the general population, genital are a frequent clinical occurrence. The aim of this study was to assess whether a connection could be demonstrated between various degrees of severity of genital and associated abnormalities. Design: All patients were classified using the Vagina, Cervix, Uterus, Adnex, and Associated Malformation (VCUAM) classification. Setting: University hospital. Patient(s): Two hundred eleven premenopausal patients with female genital. Intervention(s): The patients underwent diagnostic workup for genital using laparoscopy as well as hysteroscopy. Associated were detected by either magnetic resonance imaging (MRI) or ultrasound. Main Outcome Measure(s): Demonstration of a connection between various degrees of severity of genital and associated abnormalities. Result(s): In 72 cases (36%) out of 202 patients with uterine (VCUAM U1 4) we found associated abnormalities. The predominant findings were alterations in the renal system. When vaginal abnormality (VCUAM V1 5) alone was taken into consideration, an associated developmental disturbance in the renal tract was found in 30% of cases (n 32 from 107). Conclusion(s): A close connection was demonstrated between genital and associated abnormalities. For this reason, the diagnostic workup in patients with should always include the renal system. Depending on the severity of the clinical picture, examinations may need to be extended further. (Fertil Steril 2007;87: by American Society for Reproductive Medicine.) Key Words: Uterine malformation, genital malformation, vaginal malformation, MRKH syndrome, VCUAM classification In the general female population, genital are reported to occur with an incidence of 1% 5%, in groups of patients with fertility up to 6.5 % (1 5). The etiology is possibly due to an aberrant developmental inhibition of the Muellerian ducts during embryogenesis. To date, various genetic factors have been investigated, but a precise cause has not been identified for any of the individual types of malformation (1, 6 8). Precise classification of the individual reported in the literature is only possible from reports with sometimes small numbers of cases. Because symptoms only occur in approximately 50% of cases in connection with the, it must be assumed that mild in particular (VCUAM classification U1a 1c) are often not diagnosed and that these subgroups are underrepresented (9, 10). Figure 1 shows the distribution Received February 5, 2006; revised and accepted July 5, Reprint requests: Peter Oppelt, M.D., Department of Gynecology and Obstetrics, University Hospital, Universitaetsstrasse 21-23, D Erlangen, Germany (FAX: ; Peter.Oppelt@ gyn.imed.uni-erlangen.de of in 1,392 patients with uterine according to the review by Woelfler and Rimbach (11), using the American Fertility Society (AFS) classification (12). However, this classification did not include other associated. Regarding genital anomalies, it is usually the pathology of the uterus that is the focus of attention. Depending on their extent, these changes may occur in combination with other genital and associated. Isolated genital without changes in the uterus may also occur (13 17). Our previous publication validated a specifically group of patients with MRKH (Mayer-Rokitansky-Kuester-Hauser) and a small sample of only a few additional genital using the VCUAM Classification System defined by us (10). Therefore, the aim of the present study was to extend this validation using VCUAM to now include a total of 211 female patients with all types of genital and also test the classification in relation to associated changes (10) /07/$32.00 Fertility and Sterility Vol. 87, No. 2, February 2007 doi: /j.fertnstert Copyright 2007 American Society for Reproductive Medicine, Published by Elsevier Inc. 335
2 FIGURE 1 Distribution of uterine of 1392 patients by Woelfler and Rimbach (11). Oppelt. Female genital diagnosis. Fertil Steril MATERIALS AND METHODS Between January 2000 and June 2005, 211 patients contacted the Departments of Gynecology at the university hospitals in Erlangen and Tübingen because of sterility or genital. In a few of the patients, the data had been obtained as asymptomatic incidental findings. For precise assessment of the genital and associated anomalies, patients records, general visual examination of the urinary tract, surgical reports, x-ray pictures, magnetic resonance tomography findings, and ultrasound findings were evaluated. All patients underwent diagnostic workup for genital using laparoscopy as well as hysteroscopy and ultrasound examination of the kidneys. Symptomatic associated were then further evaluated by magnetic resonance imaging (MRI). The final classification of each malformation was carried out using the new VCUAM classification (10). This classification makes it possible to record the pathological anatomy of genital developmental disturbances descriptively. Each is recorded in accordance with the following scheme. Vagina: 0, normal; 1a, partial hymenal atresia; 1b, complete hymenal atresia; 2a, incomplete septate vagina 50%; 2b, complete septate vagina; 3, stenosis of the introitus; 4, hypoplasia; 5a, unilateral atresia; 5b, complete atresia; S1, sinus urogenitalis (deep confluence); S2, sinus urogenitalis (middle confluence); S3, sinus urogenitalis (high confluence); C, cloaca. Cervix: 0, normal; 1, duplex cervix; 2a, unilateral atresia/ aplasia; 2b, bilateral atresia/aplasia. Uterus: 0, normal; 1a, arcuate; 1b, septate, 50% of the uterine cavity; 1c, septate, 50% of the uterine cavity; 2, bicornate; 3, hypoplastic uterus; 4a, unilaterally rudimentary or aplastic; 4b, bilaterally rudimentary or aplastic. Adnex: 0, normal; 1a, unilateral tubal malformation, ovaries normal; 1b, bilateral tubal malformation, ovaries normal; 2a, unilateral hypoplasia/gonadal streak (including tubal malformation if appropriate); 2b, bilateral hypoplasia/gonadal streak (including tubal malformation if appropriate); 3a, unilateral aplasia; 3b, bilateral aplasia. Associated malformation: 0, none; R, renal system; S, skeleton; C, cardiac; N, neurologic. In any group in the VCUAM classification, the symbol can be used to indicate unclassifiable and the symbol # to indicate unknown. In the analysis, the malformation of the uterus was regarded as dominant and as the reference point in relation to other abnormalities such as those in the vagina (see Tables 1 3). In a further analytical step, the vagina was set as the reference point, as in the gynecological examination anomalies, those are noticeable first. In Table 4, the individual vaginal are correlated with additional genital and associated abnormalities. Approval for conducting basic research and compiling the relevant documentation on female genital was received through Ethics Vote no in the Faculty of Medicine at the University of Erlangen. RESULTS Among the 211 patients included in the study, 202 had uterine and 9 had isolated vaginal anomalies. Also included in this analysis for comparison were 56 patients with MRKH, previously published (10). To allow better assessment of the connection between pathological, embryological abnormalities and the associated, all of the patients were categorized, using the VCUAM classification, first with regard to their uterine changes and second, in relation to their vaginal changes. VCUAM U1 Group (Arcuate Uterus, Subseptate Uterus) Overall, only a few concomitant were found in 80 patients in this group (Table 1). Additional anomalies in the cervix were only seen in five cases. All five of these patients also had a complete septate uterus (VCUAM U1c). Among the patients included in the study, this was not observed with those in uterine categories U1a and U1b. The associated malformation described included five changes in the urogenital system, two anal atresias, one hernia, one auricular, and one cerebral artery aneurysm. Changes in the adnex area were only found in one patient, with unilateral tubal hypoplasia. VCUAM U2 Group (Bicornate Uterus) Thirty-eight patients of 202 had a bicornate uterus (Table 2). In 50% of the cases (n 19), this was accompanied by a duplex cervix. An increased proportion of in the adnex was also observed in comparison with the VCUAM U1 group. Overall, 39% of the patients had at least one associated anomaly. The largest group consisted of Oppelt et al. Female genital diagnosis Vol. 87, No. 2, February 2007
3 TABLE 1 Uterine VCUAM U1 (80 patients; 19 patients previously published in Oppelt et al.). Patient Vagina Cervix Uterus Adnex Associated Description associated Amount 1) V# C# U1a A0 M0 2) V0 C0 U1a A# M0 3) V0 C0 U1a A M0 4) V0 C0 U1a A0 MR Vesicourethral reflux 5) V0 C0 U1a A0 M0 17 x 6) V1a C0 U1a A0 M0 7) V0 C0 U1b A# M0 8) V0 C0 U1b A# M0 9) V0 C0 U1b A0 M A 10) V0 C0 U1b A0 M Malformation auricula 11) V0 C0 U1b A0 M0 37 x 12) V0 C0 U1b A0 MR B 13) V0 C0 U1b A1a M0 14) V0 C0 U1c A# MR Double ureter, B 15) V0 C0 U1c A0 MR C (left) 16) V0 C1 U1c A0 M0 17) V0 C0 U1c A0 M Cerebral aneurysm 18) V0 C0 U1c A0 M0 7 x 19) V2a C1 U1c A0 M0 2 x 20) V2b C1 U1c A0 M0 21) VC C2a U1c A0 MR Horseshoe kidney; anal atresia Note: A inguinal hernia; B unilateral renal aplasia; C double kidney. Oppelt. Female genital diagnosis. Fertil Steril changes in the urogenital system. In addition, dysplasias in the ear and nose, mental retardation, and skeletal changes were also diagnosed. VCUAM U3 Group (Hypoplastic Uterus) Only 5 of 202 patients could be assigned to this group. Four of five patients in the group showed a close association between uterine and ovarian abnormalities. Bilateral hypoplastic ovaries (gonadal streaks) were documented in all but one patient. A skeletal anomaly was present in only one case. VCUAM U4 Group (Unilaterally or Bilaterally Rudimentary Uterus) With a total of 79 of 202 patients in this group, unilateral uterine horn aplasia or a rudimentary horn (VCUAM U4a) was present in six cases (Table 3). A substantial difference was observed between the latter group and those with bilateral uterine horn aplasia/bilateral rudimentary uterine horn (VCUAM 4b) with regard to cervical involvement. Although complete vaginal atresia was present in all patients in the VCUAM U4b group, vaginal atresia was seen in only one case in the VCUAM U4a group. Three patients had no cervical pathology. A duplex cervix was present in two of the women. Overall, the VCUAM U4 major group included 11 patients with morphological changes in the adnex, ranging from unilateral tubal anomaly (VCUAM A1a) to bilateral gonadal aplasia (VCUAM A3b). At least one extragenital malformation was found in 41% (n 32) of the patients in the VCUAM U4 group. The most frequent were anomalies of the urogenital system (n 26), followed by skeletal (n 13) and heart defects (n 4). The first case of a patient with an abnormal neurologic status was also observed (n 1). VCUAM V1 5 Group (Hymenal Atresia, Septate Vagina, Stenosis of the Introitus, Hypoplasia, Atresia, Sinus Urogenitalis, Cloaca) A total of 107 from the total of 211 patients were found to have of the vagina (Table 4). Although only two of eight patients in the VCUAM V1 group had associated abnormalities, more strongly marked vaginal were more frequently combined with other changes in the genitals or associated. All women with a septate vagina (n 19) also had a duplex cervix, which continued in 14 cases with duplex uterus and in 3 cases with a complete septate uterus. In this subgroup, renal anomalies were also diagnosed in 32% of the patients (n 6), as well as mal- Fertility and Sterility 337
4 TABLE 2 Uterine VCUAM U2 (38 patients; 20 patients previously published in Oppelt et al.). Patient Vagina Cervix Uterus Adnex Associated Description associated Amount 1) V# C# U2 A# M# 2) V# C0 U2 A3b M A 3) V0 C0 U2 A# M0 2 x 4) V0 C0 U2 A# MR C (right) 5) V0 C0 U2 A# MR B 2 x 6) V0 C0 U2 A0 M0 6 x 7) V0 C0 U2 A0 MR Pelvic kidney 2 x 8) V0 C0 U2 A0 MS scoliosis 9) V0 C0 U2 A1a M0 10) V0 C1 U2 A0 M0 3 x 11) V1b C# U2 A0 M Dysmorphism ear-hand-foot, partial missing tooth germ 12) V2a C1 U2 A0 M0 3 x 13) V2a C1 U2 A0 MR B 14) V2a C1 U2 A1a M0 15) V2b C1 U2 A0 M0 4 x 16) V2b C1 U2 A0 MR B 2 x 17) V2b C1 U2 A0 MR Double renal pelvis 18) V2b C1 U2 A0 MR Ureter fissure 19) V2b C1 U2 A2a M0 20) V2b C1 U2 A2a MR B 21) V4 C1 U2 A2b M0 22) VS1 C0 U2 A0 MN Mental retardation, strabismus Note: A inguinal hernia; B unilateral renal aplasia; C double kidney. Oppelt. Female genital diagnosis. Fertil Steril formations of the adnex in 16% (two in VCUAM A2a, one in VCUAM A2b). In addition stenoses of the vaginal introitus (n 1; VCUAM V3) or vaginal hypoplasia (n 4; VCUAM V4) were basically associated with at least one additional genital change. All of the patients with complete vaginal atresia (n 72; VCUAM V5b) had simultaneous bilateral cervical aplasia as well as a bilateral rudimentary uterus or uterine aplasia. In addition, there was a marked increase in the frequency of associated anomalies in this subgroup. The most frequent of these were of the kidneys, occurring in 23 of 72 patients (32%), followed by 14 skeletal dysmorphisms (particularly in the vertebral bodies and hips). The proportion of of the adnex (n 10, 14%) and heart (n 4, 6%) was also notably high. DISCUSSION In the examination of genital, attention usually focuses primarily on changes in the uterus, and this is reflected in almost all classifications of deformation. Acien et al. (18) attempted to use an embryonic classification to document connections between genital and urologic alterations. However, the classification met with little acceptance due to the complexity involved in using it. In this present investigation we demonstrated that the VCUAM classification can now be used generally to include all female genital. The VCUAM classification, designed for easy clinical use, makes it possible to record all anatomic and associated abnormalities separately. This is very important, particularly for the description of syndromes with genital involvement. Examples include patients with MRKH, especially the MURCS syndrome (Muellerian duct aplasia, renal aplasia, and cervicothoracic somite dysplasia), which includes both genital and extragenital abnormalities (7, 19). When the individual uterine changes (VCUAM U1a U4b) are compared with the associated genital and extragenital, a connection is evident that can in part be explained on the basis of embryogenesis. For example, the close spatial relationship between the Wolffian duct (mesonephric duct) and the Muellerian duct is often regarded as explaining uterine with accompanying renal developmental disturbances. Gruenwald (20) and Magee et al. (21) were able to show that there is a direct influence of 338 Oppelt et al. Female genital diagnosis Vol. 87, No. 2, February 2007
5 TABLE 3 Uterine VCUAM U4 (79 patients; 59 patients previously published in Oppelt et al.). 1) V C1 U4a A0 MR A, silent kidney left, double aorta 2) V0 C1 U4a A# M# 3) V0 C0 U4a A0 M0 4) V0 C0 U4a A2b M0 5) V3 C0 U4a A# MR C, rectal atresia, double kidney right 6) V4 C2b U4a A M0 7) V4 C2b U4b A0 MR A, hearing loss 8) V5b C2b U4b A# M# 13 x 9) V5b C2b U4b A# M0 5 x 10) V5b C2b U4b A# MR D 11) V5b C2b U4b A# MR C 12) V5b C2b U4b A# MRC C, E 13) V5b C2b U4b A# MRS C, G, talipes varus 14) V5b C2b U4b A# MS Absence of 1/3 of the left arm 15) V5b C2b U4b A# MSN hearing loss, hypoplasia of the wrist 16) V5b C2b U4b A0 M A 17) V5b C2b U4b A0 M0 24 x 18) V5b C2b U4b A0 MC A, E 19) V5b C2b U4b A0 MR D 3 x 20) V5b C2b U4b A0 MR C 21) V5b C2b U4b A0 MR B 22) V5b C2b U4b A0 MR Malformation uretra 23) V5b C2b U4b A0 MR Horseshoe kidney 24) V5b C2b U4b A0 MRS B, malformation HWS 25) V5b C2b U4b A0 MRS A, F, high blood pressure, hypoplasia of the wrist 26) V5b C2b U4b A0 MRSC A, D, E, F 27) V5b C2b U4b A0 MS G, radial aplasia thrombocytopenia syndrome with bilateral club hand 28) V5b C2b U4b A0 MS F, cataract 29) V5b C2b U4b A1a MR B 30) V5b C2b U4b A1b MR A, B 31) V5b C2b U4b A1b MRS B, C, dwarfism, fibroma 32) V5b C2b U4b A1b MRS A, C, F 33) V5b C2b U4b A1b MRSC A, C, open duct, jaw anomaly 34) V5b C2b U4b A2a MR B 35) V5b C2b U4b A2b MRS B, F 36) V5b C2b U4b A2b MRS F, G, deformed elbow 37) V5b C2b U4b A3a M0 38) V5b C2b U4b A3a MRS B, C, F Note: A inguinal hernia; B unilateral renal aplasia; C pelvic kidney; D nephrosclerosis; E aorticopulmonary septal defect; F scoliosis; G congenital dysplasia of the hip. Oppelt. Female genital diagnosis. Fertil Steril the Wolffian duct, through induction, on the development of the Muellerian duct. A high incidence of renal abnormalities was found with uterine. Although only 5 renal abnormalities (6%) were observed in the VCUAM U1 group, 11 of the renal system were seen in the VCUAM U2 group (29%) and 25 in the VCUAM U4 group (32%). The same also applies to other associated, which are encountered most frequently in the VCUAM U4 group, particularly in connection with the MRKH syndrome. In contrast to the VCUAM groups U1, U2, and U4, only one associated malformation of the (VCUAM MS scoliosis) was observed among the five cases of the VCUAM group U3. A genetic mutation is probably not the primary factor for Fertility and Sterility 339
6 TABLE 4 Vaginal VCUAM V (107 patients; 62 patients previously published in Oppelt et al.). Patient Vagina Cervix Uterus Adnex Associated Description associated Amount 1) V1a C0 U# A# M0 2) V1a C0 U0 A0 M0 2 x 3) V1a C0 U1a A0 M0 4) V1b C# U0 A0 M0 5) V1b C0 U0 A0 M0 2 x 6) V1b C# U2 A0 M Dysmorphism ear-hand-foot, partial missing tooth germ 7) V2a C1 U0 A0 M0 8) V2a C1 U1c A0 M0 2 x 9) V2a C1 U2 A0 MR B 10) V2a C1 U2 A0 M0 3 x 11) V2a C1 U2 A1a M0 12) V2b C1 U0 A# M0 13) V2b C1 U1c A0 M0 14) V2b C1 U2 A2a MR B 15) V2b C1 U2 A0 MR B 2 x 16) V2b C1 U2 A0 MR Double renal pelvis 17) V2b C1 U2 A0 MR Ureter fissure 18) V2b C1 U2 A0 M0 4 x 19) V2b C1 U2 A2a M0 20) V3 C0 U4a A# MR C, rectal atresia, double kidney right 21) V4 C0 U0 A2b MR B 22) V4 C1 U2 A2b M0 23) V4 C2b U4a A M0 24) V4 C2b U4b A0 MR A, hearing loss 25) V5b C2b U4b A# M# 13 x 26) V5b C2b U4b A# M0 5 x 27) V5b C2b U4b A# MR D 28) V5b C2b U4b A# MR C 29) V5b C2b U4b A# MRC C, E 30) V5b C2b U4b A# MRS C, G, talipes varus 31) V5b C2b U4b A# MS absence of 1/3 of the left arm 32) V5b C2b U4b A# MSN Hearing loss, hypoplasia of the wrist 33) V5b C2b U4b A0 M A 34) V5b C2b U4b A0 M0 24 x 35) V5b C2b U4b A0 MC A, E 36) V5b C2b U4b A0 MR D 3 x 37) V5b C2b U4b A0 MR C 38) V5b C2b U4b A0 MR B 39) V5b C2b U4b A0 MR Malformation uretra 40) V5b C2b U4b A0 MR Horseshoe kidney 41) V5b C2b U4b A0 MRS B, malformation HWS 42) V5b C2b U4b A0 MRS A, F, high blood pressure, hypoplasia of the wrist 43) V5b C2b U4b A0 MRSC A, D, E, F 44) V5b C2b U4b A0 MS G, radial aplasia thrombocytopenia syndrome with bilateral club hand 45) V5b C2b U4b A0 MS F, cataract 46) V5b C2b U4b A1a MR B Oppelt. Female genital diagnosis. Fertil Steril Oppelt et al. Female genital diagnosis Vol. 87, No. 2, February 2007
7 TABLE 4 Continued. Patient Vagina Cervix Uterus Adnex Associated Description associated Amount 47) V5b C2b U4b A1b MR A, B 48) V5b C2b U4b A1b MRS B, C, dwarfism, fibroma 49) VC C2a U1c A0 MR Horseshoe kidney, anal atresia 50) VS1 C0 U2 A0 MN Anal atresia, strabismus Note: A inguinal hernia; B unilateral renal aplasia; C pelvic kidney; D nephrosclerosis; E aorticopulmonary septal defect; F scoliosis; G congenital dysplasia of the hip. Oppelt. Female genital diagnosis. Fertil Steril the hypoplastic uterus, but rather an endocrinologic failure, which in this group is likely to be found in the lack of hormone production in the ovaries (four cases of VCUAM A2b). Acien et al. (18) have attempted to infer an embryological link; however, a molecular genetic explanation has not yet been identified. Also a close relationship between the Muellerian duct and the urogenital sinus was observed. Among 107 patients with vaginal (development from the urogenital sinus, VCUAM V1 5), 90% (n 96) had cervical, 92% (n 98) had uterine, and 30% (n 32) had renal abnormalities as concomitant findings. A close association was also demonstrated in 20 patients with duplex vagina (VCUAM V2a and b) who were all diagnosed with duplex cervix. In addition, 3 cases of the 20 patients had a complete intrauterine septa and 15 patients, a duplex uteri. The connection is seen most impressively in the context of the MRKH syndrome. All 72 patients with bilateral vaginal atresia had bilateral cervical and uterine aplasia as concomitant findings (10). In contrast, when one starts primarily from the malformation that originates in the Muellerian duct, a malformation with its origin in the urogenital sinus is not found in all cases. In 202 patients with uterine (Muellerian duct; VCUAM U1 4), only 96 abnormalities of the vagina (urogenital sinus) were found. Another notable observation is the structure of the VC- UAM U2 subgroup. Among the 38 patients with bicornate uterus (VCUAM U2), no abnormalities of the cervix or vagina were found in 15 cases (40%). A further observation is that 5 (33%) of these 15 patients were suffering from of the renal system (two with pelvic kidney, two with renal agenesis, and one with unilateral double kidney). The conclusion might be that there is a direct influence of the sinus urogenitalis, through induction, on the development of the Muellerian duct and in some cases also of the Wolffian duct. Regarding all genital and their associated abnormalities it can be concluded that other superordinated induction pathways must be available for this type of abnormal development. These results contribute to the hypothesis that organogenesis primarily takes place independently, but that there are higher level regulatory mechanisms that can have common effects on both the Muellerian and Wolffian ducts and the urogenital sinus. On the basis of genetic studies in mice, particularly in the knock-out mouse model, a fundamental role in the development of the urogenital tract has been attributed to the HOXA genes. Several mouse models have shown that Hoxa10 is essential for uterine development, Hoxa11 for the caudal uterine and cervical area, Hoxa13 for the upper vagina, and Hoxa9 for the development of the fallopian tubes (22, 23). A nonsense HoxA13 mutation is known to exist in the hand foot genital syndrome in humans (24, 25). However, no mutations were found in 32 patients with Muellerian aplasia (26). In a case report of an 18-year-old woman with MRKH syndrome, Biason-Lauber et al. (27) detected a loss-of-function mutation in the WNT4 gene. The WNT4 gene appears to be important for the regulation of Muellerian duct formation and control of ovarian steroidogenesis. But genetic analyses by Clément-Ziza et al. (28) exclude WNT4 as the major responsible gene in this malformation. The question of whether MRI is capable of replacing hysteroscopy and laparoscopy in the diagnostic workup is a matter of controversy (3, 29). In our own experience, we have noted incorrect interpretations based on the MRI findings, particularly in cases of complex female urogenital malformation. Finally, it should be pointed out that female genital are frequently associated with other abnormalities. During the diagnosis of, an ultrasound examination of at least both kidneys should also be carried out in addition to the assessment of the small pelvis. The extent to which the diagnosis and workup may need to be extended further should be determined in relation to the extent of the and the patient s symptoms. In this context, clinical pictures in the areas of urology, neurology, orthopedics, and cardiology should be considered. Fertility and Sterility 341
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The VCUAM (Vagina Cervix Uterus Adnex associated Malformation) Classification: a new classification for genital malformations
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