Frequency and type of adnexal lesions in autopsy material from postmenopausal women: ultrasound study with histological correlation

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1 Ultrasound Obstet Gynecol 2003; 22: Published online in Wiley InterScience ( DOI: /uog.212 Frequency and type of adnexal lesions in autopsy material from postmenopausal women: ultrasound study with histological correlation L. VALENTIN*, L. SKOOG and E. EPSTEIN* Departments of *Obstetrics and Gynecology and Clinical Pathology, Malmö University Hospital, Lund University, Malmö, Sweden KEYWORDS: ovarian cysts; ovarian tumors; pathology; postmenopause; ultrasonography ABSTRACT Objective To determine the prevalence and histology of adnexal cysts in autopsy material from postmenopausal women. Methods The study included 104 adnexa from 52 consecutive women with a mean age of 79 (range, 64 96) years, who underwent autopsy and died from causes other than gynecological cancer or intraperitoneal cancer of extragenital origin. The adnexa were removed, put in sterile saline in separate plastic containers and examined sonographically using an 8-MHz transvaginal transducer. Each lesion detected at ultrasound examination was measured with calipers on the frozen ultrasound image and was classified according to its ultrasound morphology. The adnexa were then put in 4% formaldehyde solution and sent for histological examination. Results At ultrasound examination, 56% (29/52) of the women had adnexal lesions, cysts being detected in 54% (28/52) and solid lesions in 12% (6/52). At least one adnexal cyst with a largest diameter of 2 10 mm, > 10 mm, > 20 mm, > 30 mm and > 40 mm, respectively, was found in 33% (17/52), 21% (11/52), 12% (6/52), 8% (4/52) and 4% (2/52) of the women. The largest lesion measured 65 mm in diameter. At ultrasound examination we found 36 intra-ovarian cysts (26 inclusion cysts, three cystically degenerated corpora albicantia, five simple cysts, one serous cystadenoma and one 3-mm cyst not confirmed by the pathologist), 19 extra-ovarian cysts (all simple cysts according to the pathologist), five solid intraovarian lesions (two fibromas, one cystadenofibroma, one Brenner tumor and one case of dystrophic calcification), and one solid extra-ovarian lesion (fibroma). In addition, the pathologist detected one 20-mm solid corpus albicans, eight extra-ovarian simple cysts of 1 8 mm, and 77 intraovarian inclusion cysts of 1 4 mm. Conclusion Small ( 50 mm) benign adnexal cysts and small benign solid tumors are so common in postmenopausal women that their presence may be regarded as normal. Our results support conservative management of adnexal lesions with benign ultrasound morphology incidentally detected at ultrasound examination in postmenopausal women. Copyright 2003 ISUOG. Published by John Wiley & Sons, Ltd. INTRODUCTION With the introduction of transvaginal ultrasound examination into clinical practice, it has become evident that cysts occur quite frequently in the adnexa of asymptomatic postmenopausal women 1 5. There is still uncertainty about the likely histological diagnosis of such cysts and about how they should be managed. The aim of this study was to determine the prevalence and histology of sonographically detectable adnexal cysts in autopsy material from postmenopausal women who died from causes other than gynecological cancer or intraperitoneal cancer of extragenital origin. METHODS The study was approved by the ethics committee of the medical faculty of Lund University, Sweden. Included in the study were consecutive women 55 years old, who underwent autopsy at the Department of Pathology, Malmö University Hospital, Malmö, Sweden during the period 14 th January 2000 to 14 th February Exclusion criteria were: bilateral Correspondence to: Prof. L. Valentin, Department of Obstetrics and Gynecology, Malmö University Hospital, SE Malmö, Sweden ( lil.valentin@obst.mas.lu.se) Accepted: 12 May 2003 Copyright 2003 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER

2 Adnexal lesions at autopsy 285 oophorectomy, metastatic intraperitoneal cancer, death from gynecological cancer, previous treatment for gynecological cancer, previous pelvic radiotherapy, breast cancer diagnosis 5 years before death, tamoxifen treatment at the time of death, blood borne infectious disease (e.g. hepatitis or human immune deficiency virus) or tuberculosis. The cause of death was determined on the basis of the results of autopsy. The adnexa were removed from the body by an autopsy technician. The right and left adnexa were put in sterile saline in separate plastic containers and sent for ultrasound examination by one of two gynecologists (L.V. or E.E.). The gynecologist assessed the macroscopic appearance of each adnexa and noted the presence of any extra-ovarian cysts. Then each adnexa was examined with ultrasound, carried out with the adnexa immersed in saline in the plastic container. The ultrasound system used was a Sequoia 512 Ultrasound system (Acuson Inc., Mountain View, CA, USA) with a 5 8-MHz transvaginal transducer; the frequency used was 8-MHz in every case. The length (L), depth (D) and width (W) of each ovary were measured with calipers on the frozen ultrasound image, and ovarian volume (in ml) was calculated according to the formula: L (cm) D(cm) W(cm) 0.5. The number of cysts and solid tumors detected inside or outside each ovary was noted, and the size of each cyst or solid lesion was measured in the same manner as was ovarian size. The largest diameter of each lesion was used to characterize its size. Each lesion was classified as a unilocular cyst (a unilocular cyst without septa and without solid parts or papillary projections), a multilocular cyst (a cyst with a septum or septa but no solid parts or papillary projections), a unilocular solid cyst (a unilocular cyst containing solid parts or papillary projections but no septa), a multilocular solid tumor (a tumor with a septum or septa and solid parts or papillary projections) or a solid tumor (a tumor in which the solid components comprised 80% or more of the tumor) 6,7. The presence of papillary projections, defined as any solid projections into a cyst cavity from the cyst wall with a height 3mm 8, was noted. The results of the ultrasound examinations were documented on hard copies and magnetic optic discs. After completion of the ultrasound examination, the adnexa were put in 4% formaldehyde solution and sent for histological examination by the team pathologist (L.S.). All available material was embedded in paraffin and stained with hematoxylin-eosin and Masson s trichrome stain. Each ovary was sectioned sagittally by the pathologist. At least two sections of each ovary were examined under contact reticles (Leitz Periplan 5x/18 MP, Stuttgart, Germany). Each intra- or extra-ovarian lesion was measured using a slide gauge, the largest diameter of the lesion being used to characterize its size. The pathologist had complete knowledge of the ultrasound findings (ovarian size and size, morphology and location of any adnexal lesion) when performing the examinations. By comparing the size, morphology and location of any lesion detected at the pathological examination of the specimen with those of any lesion detected at the ultrasound examination of the same specimen, the pathologist was able to identify with reasonable certainty each lesion seen at ultrasound examination and to assign to it a correct histopathological diagnosis. Cysts with flat or cuboid epithelium and with a largest diameter 10 mm were assigned a histological diagnosis of inclusion cyst 9, whereas cysts with flat or cuboid epithelium and with a largest diameter > 10 mm were assigned a diagnosis of simple cyst, irrespective of their macroscopic appearance and ultrasound morphology 9. Statistical analyses were carried out with the aid of a Macintosh computer using the Statview 4.5 TM statistical program (Abacus Concepts, Inc., Berkeley, CA, USA, ). Wilcoxon s test was used to test the statistical significance of differences in paired continuous data, and Fisher s exact test was used to test the statistical significance of differences in unpaired categorical data. Two-tailed P-values are given with 5% as the level of significance. RESULTS One hundred and ten adnexa from 55 consecutive women fulfilling the inclusion criteria were sent for ultrasound examination. Of these, three were excluded because the specimen was mummified because of incomplete closure of the formaldehyde container. Thus, 104 adnexa from 52 consecutive women were included. The mean ± SD age of the women included was 79 ± 8.0 years, with a median of 79.5 years and a range of years. The causes of death were coronary or vascular disease including stroke (n = 23), pulmonary embolism (n = 9), extragenital cancer (n = 8), hemorrhagic shock (n = 4) or other (n = 8). At ultrasound examination, 56% (29/52) of the women had adnexal lesions, cysts being detected in 54% (28/52) and solid lesions in 12% (6/52). Eight percent (4/52) of the women had multilocular or multilocular solid cysts. The findings of the ultrasound examiner are summarized in Table 1. One third of all women (17/52) had at least one adnexal cyst with a diameter of 2 10 mm, 21% (11/52) had at least one adnexal cyst > 10 mm, 12% (6/52) had at least one adnexal cyst > 20 mm, 8% (4/52) had at least one adnexal cyst > 30 mm, and 4% (2/52) had at least one adnexal cyst > 40 mm. Among the 29 women with adnexal lesions at ultrasound examination we found 36 intra-ovarian cysts, 19 extra-ovarian cysts, five solid intra-ovarian lesions and one solid extra-ovarian lesion. The 36 intra-ovarian cysts comprised 30 unilocular cysts with a diameter of 2 10 mm and six cysts with various ultrasound morphologies and a diameter of mm. Papillary projections were not detected in any lesion. Details of the sonographically detected intra-ovarian cysts including their histology are given in Table 2. The solid intraovarian lesions detected at ultrasound examination are described in Table 3. They comprised two fibromas (12 mm and 25 mm), one cystadenofibroma (20 mm),

3 286 Valentin et al. Table 1 Numbers of women with and without adnexal lesions according to ultrasound examiner and pathologist Ultrasound examiner Pathologist No adnexal lesions (n (%)) 23 (44) 11 (21) Unilateral ovarian lesions with or 13 (25) 16 (31) without extra-ovarian lesions (n (%)) Bilateral ovarian lesions with or without 11 (21) 23 (44) extra-ovarian lesions (n (%)) Extra-ovarian lesions only (n (%)) 5 (10) 2 (4) Total 52 (100) 52 (100) Table 2 Cystic ovarian lesions detected at sonography and their histological characteristics Cyst size (mm) Women (n (%))* 18 (35) 3 (6) 2 (4) Lesions (n) Unilocular Multilocular Multilocular solid Histology (n) Inclusion cyst Cystically degenerated corpus albicans Simple cyst Serous cystadenoma *Refers to women with largest cyst size 2 10 mm, mm or mm. One 3-mm unilocular cyst, which could have been an inclusion cyst or a cystically degenerated corpus albicans, was not confirmed by the pathologist. The serous cystadenoma was multilocular. Table 3 Solid ovarian lesions detected at sonography and their histological characteristics Size of lesion (mm) Women (n (%))* 1 (2) 3 (6) 1 (2) Lesions (n) Histology (n) Dystrophic calcification Fibroma, cystadenofibroma Brenner tumor *Refers to women with largest lesion 2 10 mm, mm and mm. Table 4 Extra-ovarian lesions detected at sonography and their histological characteristics Size of lesions (mm) Women (n (%))* 4 (8) 4 (8) 2 (4) Lesions (n) Unilocular Multilocular Solid Histology (n) Simple cyst Fibroma *Refers to women with largest lesion 2 10 mm, mm and mm. simple cysts because they were lined with flat cuboid epithelium. The findings of the pathologist are summarized in Table 1. In addition to the lesions found at ultrasound examination, the pathologist detected one 20-mm solid corpus albicans, eight extra-ovarian unilocular simple cysts (six with a diameter of 1 2 mm, one with a diameter of 4 mm, and one with a diameter of 8 mm), and 77 unilocular intra-ovarian inclusion cysts (63 with a diameter 1 mm, eight with a diameter of mm, five with a diameter of mm, and one with a diameter of 4 mm). According to the pathologist 48% (25/52) of the left ovaries and 52% (27/52) of the right ovaries contained no inclusion cysts, 46% (24/52) of the left ovaries and 40% (21/52) of the right ovaries contained one to three inclusions cysts, and 6% (3/52) and 8% (4/52), respectively, contained four or more inclusion cysts. The ultrasound morphology and the histology of the ovarian lesions did not differ between women with unilateral and those with bilateral ovarian lesions. This was true irrespective of whether unilateral and bilateral were defined on the basis of ultrasound findings or on the basis of histopathological findings. Ovarian size as measured by ultrasound is shown in Table 5. When measured by ultrasound, normal postmenopausal ovaries had a size of approximately cm. All three women excluded because of mummified adnexa had intra-ovarian lesions at ultrasound examination. One woman had cysts in both her ovaries (largest diameter, 8 mm), one woman had two cysts in her left ovary (62 mm and 22 mm) and the third woman had a 42-mm solid lesion in her right ovary. one Brenner tumor (35 mm) and one case of dystrophic calcification (9 mm). Details of the 20 extra-ovarian lesions seen at ultrasound examination are given in Table 4. They consisted of 18 unilocular cysts with a diameter of 3 23 mm, one multilocular cyst with a diameter of 34 mm, and one 35-mm solid fibroma. The extra-ovarian cysts were classified by the pathologist as DISCUSSION It was not possible for us to determine the age at menopause of the women included, but because the youngest woman was 65 years old, we feel confident that all women were several years postmenopausal. Despite the women included being likely to represent a selected group

4 Adnexal lesions at autopsy 287 Table 5 Ovarian size as measured by ultrasound Right ovary Left ovary P No intra-ovarian lesions, or lesions 10 mm at ultrasound examination* Length (mm, median (range)) 26 (15 36) 24 (16 42) 0.42 Width (mm, median (range)) 10 (6 16) 9 (4 19) Depth (mm, median (range)) 16 (6 29) 15 (7 23) 0.03 Volume (ml, median (range)) 1.9 ( ) 1.8 ( ) No intra-ovarian lesions at ultrasound examination Length (mm, median (range)) 26 (15 34) 24 (16 42) 0.57 Width (mm, median (range)) 10 (6 16) 9 (4 19) Depth (mm, median (range)) 16 (6 29) 15 (11 23) 0.38 Volume (ml, median (range)) 2.0 ( ) 1.7 ( ) 0.02 Wilcoxon s test was used throughout. *48 left ovaries, 46 right ovaries, 43 pairs of ovaries. 32 left ovaries, 36 right ovaries, 27 pairs of ovaries. In one woman, the left ovary was so small that it was not identified at ultrasound examination. with very healthy adnexa (because one would expect most diseased adnexa causing symptoms to have been removed before death), adnexal lesions were common. The ultrasound examiners found 56% of the women to have adnexal lesions and 46% to have ovarian lesions, the corresponding figures for the pathologist being 79% and 75%. Most lesions were cystic, but as many as 12% of the women had solid lesions detected at ultrasound examination, all solid lesions being confirmed by the pathologist. The discrepancy between the findings of the ultrasound examiner and those of the pathologist can be explained by all but one of the 71 inclusion cysts 2 mm found by the pathologist remaining undetected at ultrasound examination. The reason why they remained undetected is almost certainly limited resolution of the ultrasound system. Inattentiveness of the ultrasound examiner probably explains why eight cysts mm seen by the pathologist were not detected at ultrasound examination. It might not be possible to detect even large solid corpora albicantia at ultrasound examination. The results of the present autopsy study support the suggestion that small ( 50 mm) benign cystic adnexal lesions are so common in postmenopausal women that they should be regarded as normal, as do the results of in-vivo studies examining the prevalence of adnexal cysts incidentally detected at ultrasound examination in asymptomatic postmenopausal women. Reported prevalences range between 21% (cyst size not stated) 10, 17% (cyst size, 3 47 mm) 1, 7% ( simple cysts, mm) 5 and 6% (minimum cyst size not stated) 4. In some of these studies a small proportion of the women might not have been postmenopausal 4,5,10.Most of the cysts in the studies cited were simple cysts, i.e., unilocular, anechoic cysts with smooth walls. However, complex, benign cysts were found in 2% 1 and 3% 4 of the women, and complex and presumably benign (incomplete follow-up) cysts in 5% 10. In one of our own ultrasound studies of asymptomatic postmenopausal women, we found adnexal cysts with benign ultrasound morphology with a diameter of 4 31 mm in 17% (25/148) of the women. Most of these lesions were unilocular cysts, but two women (1.3%) had multilocular cysts that were benign according to their clinical course, and one woman (0.7%) had a benign solid lesion (published and unpublished results from the study published in ). The cysts in the present in-vitro autopsy study seem to have been larger than those in our in-vivo study; 21% of the women in the present autopsy study had at least one cyst > 10 mm vs. 9% of those in our in-vivo study, 12% vs. 3% had at least one cyst > 20 mm, and 8% vs. 0.6% had at least one cyst > 30 mm (unpublished results from the 1995 study 2 ). Moreover, benign solid lesions were much more common in the present autopsy study than in our in-vivo study (12% vs. 0.7%) as were benign complex cystic lesions (8% vs. 1.3%) (unpublished results from the 1995 study 2 ). Perhaps the difference is to be explained by the women in the present autopsy study being older than those in our in-vivo study (median age, 79.5 years vs. 54 years); a larger number of cysts and solid tumors mayhavehadtimetodevelopandtoincreaseinsizeinthe older women. Another possible explanation of the greater proportion of women with adnexal lesions in the present autopsy study is that lesions may have been easier to detect in vitro. There may also be technical explanations for the greater proportion of women with complex cysts in the present autopsy study than in studies carried out in vivo 1,2,4,10. Thin septa and small solid parts might be easier to detect in vitro than in vivo. However, easier detection in vitro is unlikely to explain the larger size of the lesions in the present autopsy study than those in our in-vivo study. Only one of the women in the present autopsy study had undergone gynecological ultrasound examination at our institution before she died. The invivo examination showed a 3-cm unilocular cyst in the right adnexa which we believed to be an ovarian cyst. The in-vitro examination revealed a normal right ovary with a 34-mm extra-ovarian cyst with thin septa and three locules. Even though it would be very interesting to conduct a study in which asymptomatic postmenopausal women were examined with transvaginal ultrasound and then had their adnexa examined at subsequent autopsy, such a study would be extremely difficult to carry out in practice. The number of inclusion cysts detected by our pathologist is lower than that in a study by Mittal and coworkers 11, in which 21% of normal ovaries (used as

5 288 Valentin et al. Table 6 Studies on expectant management of cysts with benign ultrasound morphology incidentally detected at ultrasound examination of postmenopausal women Reference Cysts (n) Cyst type Cyst size (mm) Follow-up (years) Valentin & Akrawi (2002) Benign-looking Levine et al. (1992) 1 72 Simple Kroon & Andolf (1995) Simple? Andolf & Jörgensen (1988) Benign-looking Aubert et al. (1998) Simple Goldstein et al. (1989) Simple? Auslender et al. (1996) Simple Bailey et al. (1998) Simple 100 (90% 50) Conway et al. (1998) Simple Not stated Overall 754 Mostly simple Most 50 mm Several years controls for women with ovarian cancer) contained four or more inclusion cysts vs. only 6 8% of the ovaries in our study. Differences in patient selection and study design might explain this discrepancy. The results of a large number of studies support the safety of conservative management of adnexal cysts with benign ultrasound morphology incidentally detected at ultrasound examination in postmenopausal women 1,4,5, We found seven published studies in which a total of 333 postmenopausal women with 382 adnexal cysts with benign ultrasound morphology incidentally detected at ultrasound examination were followed for up to 9 years without any signs of the cysts being malignant at detection or becoming malignant 1,12 17 during follow-up (Table 6). In addition, Bailey et al. 4 and Conway et al. 5 sonographically followed 256 and 116 simple cysts in asymptomatic women stated to be postmenopausal or 50 years old. They found no evidence that any of the cysts was malignant at detection or became malignant during follow-up. However, some of the women in their studies might not have been postmenopausal, because Bailey et al. 4 included women 50 years old without regard to menopausal status, and Conway et al. 5 did not define postmenopausal status. We believe that the results of the present autopsy study lend further support to conservative management of adnexal cysts 50 mm with benign ultrasound morphology incidentally detected at ultrasound examination in postmenopausal women. Moreover, our results suggest that solid benign adnexal lesions 50 mm are common and may be regarded as normal findings in older postmenopausal women. Results for ovarian volume as measured by transvaginal ultrasound in postmenopausal women in vivo vary between studies from a mean/median of 1.1 ml to 2.5 ml 2,10, The differences are probably to be explained by differences in age and number of years past menopause, because ovarian volume as measured by transvaginal ultrasound decreases with both The differences may also be explained by some studies including only ovaries without ovarian cysts 2,21, some including ovaries with small cysts 20, and some not stating whether ovaries with cysts were included 18,19,22. Weight, parity and a history of hormone replacement therapy may also affect ovarian size 23, and ethnicity may play a role. The ovarian volumes in the present in-vitro study fall within the range of results obtained in most invivo ultrasound studies We found the right ovary to be significantly larger than the left one, but the difference was so small as to be almost certainly clinically irrelevant. In-vivo ultrasound studies found no differences in size between the right and left ovaries 2,19,22. Boss et al. 24 reported that senescent ovaries removed from the body at autopsy had a size of cm, or cm. It is not clear exactly how the measurements were taken, nor whether they were taken on fresh ovaries or on ovaries fixed in formaldehyde, but these sizes are slightly smaller than those obtained at ultrasound examination in our study. We did not compare measurements of ovarian size taken by our ultrasound examiners on the fresh specimens with those taken by our pathologist on the formaldehyde fixed specimens; shrinkage of specimens after formaldehyde fixation makes such a comparison inappropriate. In summary, the present autopsy study shows that small benign adnexal cysts and small benign solid adnexal lesions are so common in postmenopausal women who die from causes other than gynecological cancer or intraperitoneal cancer of extragenital origin, that their presence may be regarded as normal. Our study is one among many others 1,4,5,10,12 17,25 that indirectly support conservative management in postmenopausal women of adnexal lesions with benign ultrasound morphology incidentally detected at ultrasound examination. ACKNOWLEDGMENTS The study was supported by grants from funds administered by the Malmö Health Care Administration, a government grant for clinical research (ALF-medel and Landstingsfinansierad regional forskning), Allmänna Sjukhusets i Malmö Stiftelse för bekämpande av cancer, and the Swedish Medical Research Council (grants nos. B96-17X A, K98-17X A, and K X A).

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