Pelvic Ultrasonography in Turner Syndrome: Standards for Uterine and Ovarian Volume
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1 Pelvic Ultrasonography in Turner Syndrome: Standards for Uterine and Ovarian Volume Hans P. Haber, MD, Michael B. Ranke, MD The purpose of this study was to investigate uterine and ovarian size according to age and pubertal stage in patients with Turner syndrome. Ultrasonographic evaluation of the uterus and the ovaries was performed in 93 patients with Turner syndrome, aged 12 days to years. The data were compared with those of 190 healthy controls. One or both ovaries were detected in 41 of 93 patients (44%). Within the prepubertal group, mean uterine volume and mean ovarian volume of the patients with Turner syndrome were significantly (P < 0.001) lower than those of controls (0.5 ± 0.2 ml versus 1.0 ± 0.3 ml; 0.3 ± 0.3 ml versus 0.6 ± 0.4 ml, respectively). In prepubertal girls, no significant relationship was found between age and uterine size or ovarian size. Both uterine volume and ovarian volume of 19 women with spontaneous puberty increased during breast development, although mean uterine volume and mean ovarian volume were significantly (P < 0.01) lower than those of pubertal control patients. KEY WORDS: Turner syndrome; Pelvis, ultrasonography; Uterus, volume; Ovary, volume. ABBREVIATIONS TS, Turner syndrome; AP, Anteroposterior; SD, Standard deviation; ANOVA, Analysis of variance Received July 28, 1998, from the Department of Pediatrics, University of Tübingen, Tübingen, Germany. Revised manuscript accepted for publication January 13, Address correspondence and reprint requests to H. P. Haber, MD, Department of Pediatrics, University of Tübingen, Hoppe-Seyler- Strasse 1, D Tübingen, Germany. Turner syndrome is a chromosomal disorder characterized by a variety of physical abnormalities, such as short stature, webbed neck, cubitus valgus, and sexual infantilism. 1 A common feature of the patients is gonadal dysgenesis, resulting in the absence of normal gonadal development during fetal and postnatal life. In recent years, advances in ultrasonographic imaging of the pelvic organs have extended our knowledge about normal gonadal maturation. 2,3 High-resolution transducers now allow the visualization of ovarian structures even in some TS patients. 4 6 It has been demonstrated that, during childhood, ovaries range in appearance from streak ovaries containing fibrous tissue devoid of ovarian follicles to gonads having normal morphology and function. 7 Recently investigations have indicated the prognostic value of ovarian sonographic scans in predicting the sexual development of girls with TS. 8 To date, only limited information is available on the uterine development of these patients, 4,5,9 and standards for sonographic measurements have not yet been established. Our aim was to perform pelvic sonography in girls and women with TS in order to obtain reference data for uterine and ovarian volume in this diagnostic group by the American Institute of Ultrasound in Medicine J Ultrasound Med 18: , /99/$3.50
2 272 OVARIAN AND UTERINE VOLUME IN TURNER SYNDROME J Ultrasound Med 18: , 1999 MATERIAL AND METHODS Between 1990 and 1996, a total of 93 TS patients (age range, 12 days to years; mean, 9.88 years) were investigated. The study group included 71 prepubertal patients (age range, 12 days to years; mean, 8.80 years) and 19 girls with spontaneous development of puberty (age range, to years; mean, years). The control group consisted of 190 healthy girls ranging in age from 1 day to 17 years (mean, 4.95 years). Among them were 158 prepubertal (mean age, 3.40 years) and 32 pubertal (mean age, years) girls. The girls were either the healthy siblings of patients we scanned or other patients either being followed for urinary tract infections or obstipation or being examined for suspicion of other minor, nonendocrinologic but acute disease. The data concerning 178 subjects in this group were described in a previous report. 10 All patients displayed the phenotypic features common to TS. The chromosomal diagnosis was made using cultured peripheral blood lymphocytes. The karyotype distribution is listed in Table 1. Among the prepubertal girls with TS, 46 of 74 (62%) had the 45,X karyotype, whereas 28 of 74 (38%) had variant karyotypes. In the pubertal group, 18 of 19 (95%) patients had variant karyotypes. Pubertal staging was done according to the Tanner scale. 11 Ten of the pubertal patients with TS had breast stage B 2 and nine had breast stage B 3 4. The sonographic examinations were carried out at presentation and prior to treatment, in order to identify anomalies of the renal tract. Informed consent was obtained either from a parent or from both parent and subject, for both patients and controls. Ultrasonographic examination was performed according to the conventional full-bladder technique, using a 5 or 7 MHz real-time sector scanner (Acuson 128, Mountain View, CA). All scans were obtained by the same examiner, the objective being to minimize interobserver variation. A standard Table 1: Karyotypes of Patients with Turner Syndrome in Relation to Pubertal Development Karyotype Prepubertal Pubertal No. of Cases 45,X 46 1 X mosaicism 13 6 Isochromosomes 8 10 Ring chromosomes 2 2 X deletions 5 0 Total imaging protocol was followed. Measurements of the uterus and the ovary were done in transverse, AP, and longitudinal planes. The maximum values for each of these planes were the basis of our calculations (Fig. 1). The volume of the uterus and the ovary was calculated using the formula of a prolate ellipsoid: Volume = Transverse AP L The mean value of the right and left ovaries was calculated if both were detectable. The values were expressed as mean ± SD. All statistical analyses were performed with JMP software (SAS Institute, Cary, NC). Regression analysis and ANOVA were used in identifying correlations among age, uterine length, uterine volume, and ovarian volume in the control and patient groups. The chi-square test (Pearson test) was used in testing for significant differences between ovarian visibility and the distribution of karyotypes among the controls and patient groups. The level of statistical significance was set at RESULTS Uterine Size Ultrasonographic data for all the subjects and patients studied are given in Tables 2 and 3. The distribution of uterine volume, according to chronologic age and pubertal development, is shown in Figure 2, in a comparison with the normal range in healthy controls. Figure 3 shows the 5th, 50th, and 95th percentiles for uterine volume in TS in relation to age. Prepubertal Girls As with the controls, the highest values were measured in the neonate group and also in pubertal girls. In the first 2 months of life, the mean uterine length and mean uterine volume were 33 ± 6 mm and 3.2 ± 1.6 ml, respectively. Neither the mean uterine length nor the mean uterine volume differed significantly from age-matched control values, being 34 ± 5 mm and 3.0 ± 1.6 ml, respectively. After the first months of life, we observed a sharp decline in length and volume to the normal prepubertal range. In prepubertal girls between 3 months and 16 years, no significant correlation exists between uterine size and chronologic age (Fig. 2). Mean uterine length and mean uterine volume in the prepubertal girls with TS were 26 ± 5 mm and 0.5 ± 0.2 ml, respectively. Mean uterine length and mean uterine volume in the prepubertal control subjects were 29 ± 4 mm and 1.0 ± 0.3 ml, respectively. The
3 J Ultrasound Med 18: , 1999 HABER AND RANKE 273 differences between the two groups were statistically significant (P < 0.001). The mean uterine length and mean uterine volume in girls with the 45,X karyotype were both lower than those in the variant karyotype group (25 ± 5 mm versus 27 ± 5 mm, and 0.4 ± 0.2 ml versus 0.6 ± 0.2 ml, respectively). However, only the difference in mean uterine volume proved to be statistically significant (P < 0.05). Pubertal Subjects and Patients In pubertal subjects and patients, we observed an increase in uterine size (Fig. 2). Both mean uterine length and mean uterine volume were higher in breast stage B 3 4 (56 ± 14 mm and 8.3 ± 6.4 ml, respectively) than in stage B 2 (38 ± 5 mm and 2.3 ± 1.2 ml, respectively). The differences between the two groups were significant at a P value of less than and 0.01, respectively. In pubertal control subjects, mean uterine length and mean uterine volume were 40 ± 5 mm and 2.4 ± 0.6 ml at breast stage B 2, and 64 ± 10 mm and 15.9 ± 9.7 ml at breast stage B 3 4, respectively. Although mean values in TS were lower than those in control subjects, a statistically significant difference between the two groups was noticed only in stage B3 4 (P < 0.05 and 0.01, respectively). When subjects and patients in pubertal stage B 2 and B 3 4 were consid- Figure 1 A, B, Sagittal (A) and axial (B) scans from a 14 year old girl with 45,X karyotype demonstrate a small uterus (length, 22 mm; volume, 0.2 ml). C, Sagittal scan of the streak ovary (volume < 0.1 ml) from the same patient. D, Axial scan of an ovary of normal size and microcystic structure in a 4 year old girl with 45,X/46,XX karyotype (distance between the two marks, 26 mm). Distances between the grading lines, 5 mm. A B C D
4 274 OVARIAN AND UTERINE VOLUME IN TURNER SYNDROME J Ultrasound Med 18: , 1999 Table 2: Uterine Volume (Mean ± SD) in Relation to Age and Pubertal Stage in Turner Syndrome and Controls Turner Syndrome Controls Age Number Uterine Length Uterine Volume Number Uterine Length Uterine Volume Pubertal Stage (B*) (yr) (n) (mm) (ml) (n) (mm) (ml) B ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.3 B ± ± ± ± 0.6 B ± ± ± ± 9.7 *Breast stage. No prepubertal controls were included in this age group. ered together, we found a significant (P < 0.01) difference between the mean uterine volume of the TS group (5.1 ± 5.3 ml) and that of control subjects in the corresponding pubertal stage (11.6 ± 10.2 ml). Ovarian Size One or both ovaries were detected in 41 of 93 study participants (44%). Table 3 lists the frequency of detected ovaries according to age and pubertal stage. Figure 4 shows ovarian volume according to age. A significant relationship was found between karyotype and visualization of ovaries (P < 0.05). Patients with the 45,X karyotype had the lowest percentage (34%), whereas those with variant karyotypes had the highest percentage (54%) of detectable ovaries. The mean ovarian volume in patients with the 45,X karyotype was lower than that in those with variant karyotype (0.2 ± 0.2 ml versus 0.4 ± 0.3 ml, respectively). However, the difference between the two groups was not statistically significant. Prepubertal Girls In girls older than 4 months and younger than 16 years of age, we found a significant (P < 0.05) progressive decline in the percentage of detectable ovaries. Table 3 gives mean ovarian volume values for the various age groups. In prepubertal girls, no significant correlation was found between age and ovarian volume (Fig. 4). In these participants, mean ovarian volume was 0.3 ± 0.3 ml. In prepubertal control girls, mean ovarian volume was 0.6 ± 0.4 ml. The difference between the two groups was statistically significant (P < 0.001). Pubertal Subjects and Patients The rate of ovary visualization was significantly (P < 0.01) higher in pubertal subjects and patients (74%) than in prepubertal girls (37%). Ovary volume according to age is depicted in Figure 4. During puberty a significant (P < 0.001) increase in ovarian volume occurred. The mean ovarian volume in pubertal patients with TS, as a group, was 1.4 ± 1.0 Table 3 Ovarian Volume (Mean ± SD) and Ovarian Visibility in Relation to Age and Pubertal Stage in Turner Syndrome and Controls Turner Syndrome Controls Age Number Ovarian Visibility Ovarian Volume Number Ovarian Volume Pubertal Stage (B*) (yr) (n) (%) (ml) (n) (ml) B ± ± ± ± ± ± ± ± B ± ± 0.9 B ± ± 2.4 *Breast stage. Percentage frequency of detectable ovaries. No controls were present in this age group.
5 J Ultrasound Med 18: , 1999 HABER AND RANKE 275 ml, versus 3.8 ± 2.6 ml in corresponding pubertal stages for the control group. The difference between the two groups was statistically significant (P < 0.001). When study participants in pubertal stages B 2 and B 3 4 were considered separately, a statistically significant (P < 0.001) difference between TS and controls could be found only in stage B 3 4. DISCUSSION Ultrasonography has been shown to be useful in the evaluation of pediatric patients with endocrine disorders. 3,12 We therefore employed this method in determining uterine and ovarian size in girls with Turner syndrome. In this study, we present reference values for uterine and ovarian size, which were measured in subjects and patients ranging in age between 12 days and 18 years. In our study population, uterine volume decreased after birth and remained low until about 10 years of age. This postnatal decline also has been observed in healthy girls and possibly reflects the clearing of maternal estrogens after birth. 3 In contrast, our data indicate that ovarian volume remains unchanged from the neonatal age to early childhood. However, the relevance of this finding is limited because our study included only a small number of participants in this age group. At the time of onset of pubertal development in the patients and subjects Figure 2 Uterine volume obtained after logarithmic transformation according to age in 93 patients with TS. Open circles indicate data for prepubertal girls; solid circles indicate date for patients with spontaneous pubertal development. Lines indicate 5th, 50th, and 95th percentiles based on measurements obtained in 190 healthy girls. we studied, we observed that uterine and ovarian volume increased progressively. This confirmed the results reported by Mazzanti and coworkers. 8 Our data show that, for all age groups, ranging from 0.25 to 18 years, uterine volume was lower than that in healthy controls. This indicates uterine hypoplasia in girls with TS. A similar finding was reported by Mazzanti and colleagues, 8 although these authors did not quote specific values. In contrast, in one series of 79 patients with TS who were older than 10 years of age, uterine length did not differ from that of age-matched controls. 6 This was not confirmed by Shawker and coauthors, 5 who observed short uterine length in six of 11 (55%) sexually infantile patients. However, in both studies, uterine volume was not determined. In our study, the impairment in uterine volume was more marked than that of uterine length, a finding which suggests that the difference in uterine volume was due mainly to reduced uterine thickness rather than abnormally short uterine length. Our study showed that, in patients with spontaneous breast development, a higher rate of visualization of the ovaries was achieved than in prepubertal girls. This confirms the reports of others, in which successful imaging was achieved mainly after spontaneous puberty in girls with nonstreak ovaries. 6,8 Moreover, it has been demonstrated that a higher prevalence of spontaneous breast development occurred in patients with variant karyotypes than among those with 45,X karyotype. 13 In fact, 18 of 19 (95%) of our patients with spontaneous breast development had variant karyotypes. Thus, it has been Figure 3 Uterine volume calculated from logarithmic transformation according to age in 93 patients with TS. Lines indicate 5th, 50th, and 95th percentiles.
6 276 OVARIAN AND UTERINE VOLUME IN TURNER SYNDROME J Ultrasound Med 18: , 1999 REFERENCES Figure 4 Ovarian volume according to age in 41 TS patients with detectable ovaries. Open circles indicate data for prepubertal girls; solid circles indicate data for patients with spontaneous pubertal development. Lines indicate 5th, 50th, and 95th percentiles. suggested that ovarian visualization linked with karyotype pattern may be a useful tool in predicting residual ovarian function and, therefore, may have prognostic value in terms of the sexual development of patients. 6,8 However, in some cases, ovarian visualization did not correlate with ovarian function. 8 As there is a close correlation between uterine volume and estradiol serum concentrations, 2,5 uterine size may be an indicator of endogenous estrogen production or prior exogenous administration of estrogen. Longitudinal studies are necessary to clarify whether sonographic measurement of uterine volume provides additional information about continuing ovarian function and, therefore, may be helpful in identifying patients who need not be given estrogen treatment to initiate the development of secondary sexual characteristics. This is particulary important with regard to the patient s final height, because estrogen administration is known to have a negative effect on growth by its involvement in bone age advancement. 14 If treatment is necessary subsequently, when germ cell loss progresses, pelvic ultrasonography may be a useful tool for monitoring the effect of estrogen treatment. For this purpose, knowledge of normal uterine size in TS is a prerequisite in correctly interpreting sonographic measurements. 1. Turner HH: A syndrome of infantilism, congenital webbed neck and cubitus valgus. Endocrinology 23:566, Salardi S, Orsini LF, Cacciari E, et al: Pelvic ultrasonography in premenarchal girls: Relation to puberty and sex hormone concentrations. Arch Dis Child 60:120, Ivarsson SA, Nilsson KO, Persson PH: Ultrasonography of the pelvic organs in prepubertal and postpubertal girls. Arch Dis Child 58:352, Kalifa G, Sellier N, Rouxel A, et al: Pelvic ultrasonography in Turner syndrome. J Belge Radiol 70:299, Shawker TH, Garra BS, Loriaux DL, et al: Ultrasonography of Turner s syndrome. J Ultrasound Med 5:125, Massarano AA, Adams JA, Preece MA, et al: Ovarian ultrasound appearances in Turner syndrome. J Pediatr 114:568, Lippe B, Westra SJ, Boechat MI: Ovarian function in Turner syndrome: Recognizing the spectrum. In Hibi I, Takano K (Eds): Basic and Clinical Approach to Turner Syndrome. New York, Elsevier Science Publishers, 1993, p Mazzanti L, Cacciari E, Bergamaschi R, et al: Pelvic ultrasonography in patients with Turner syndrome: Age-related findings in different karyotypes. J Pediatr 131:135, Rosenberg D, Tell G: Syndrome de Turner: A propos d une statistique de 60 observations. Pediatrie 27:831, Haber HP, Mayer EI: Ultrasound evaluation of uterine and ovarian size from birth to puberty. Pediatr Radiol 24:11, Tanner JM, Whitehouse RH: Clinical longitudinal standards for height, weight, height velocity, weight velocity and stages of puberty. Arch Dis Child 51:170, Salardi S, Orsini LF, Cacciari E, et al: Pelvic ultrasonography in girls with precocious puberty, congenital adrenal hyperplasia, obesity, or hirsutism. J Pediatr 112: 880, Park E, Bailey JD, Cowell CA: Growth and maturation of patients with Turner s syndrome. Pediatr Res 17:1, Ranke MB: Growth disorder in the Ullrich-Turner syndrome. Baillieres Clin Endocrinol Metab 196:603, 1992
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