International Journal of Gynecology & Obstetrics 74 Ž2001. 45᎐50
Article
Relationship between age, histological type, and size of ovarian tumors K. Okugawaa,U , T. Hirakawaa , K. Fukushimaa , T. Kamurab, S. Amadaa , H. Nakano a a
Department of Obstetrics and Gynecology, Graduate School of Medical Sciences, Kyushu Uni¨ ersity, Fukuoka, Japan b Department of Obstetrics and Gynecology, Kurume Uni¨ ersity School of Medicine, Kurume, Japan Received 17 November 2000; received in revised form 27 March 2001; accepted 4 April 2001
Abstract Objecti¨ e: To clarify the relationship between age, histological type, and size of ovarian tumors. Method: A review was made of 1648 cases of histopathologically diagnosed ovarian tumors and tumor-like lesions, and information on the age of the patients and size of the tumor was obtained. Statistical analysis was performed using Kruskal᎐Wallis tests or Mann᎐Whitney U-tests. Results: There were 840 Ž51%. cases of benign tumors, 73 Ž4%. cases of tumors of low malignant potential ŽLMP., 268 Ž16%. cases of malignant tumors and 467 Ž28%. cases of tumor-like lesions. The age of the patients was significantly different among tumor-like lesions Ž34.6" 8.1 years., benign tumors Ž39.8" 16.4 years., LMP tumors Ž45.2" 18.3 years. and malignant tumors Ž51.9" 13.0 years. Ž P- 0.0001.. The maximum diameter of the tumors was significantly different among tumor-like lesions Ž7.1" 3.3 cm., benign tumors Ž10.9" 5.6 cm., malignant tumors Ž13.6" 6.5 cm. and LMP tumors Ž18.5" 6.8 cm. Ž P- 0.0001.. Conclusion: The distribution of tumor histological type Žtumor-like lesions, benign, LMP and malignant. was correlated against patient age and lesion diameter, with tumors in older patients or larger tumors more likely to be malignant. 䊚 2001 International Federation of Gynecology and Obstetrics. All rights reserved. Keywords: Ovarian tumor; Histological type; Age; Size; Japan
U
Corresponding author. Department of Obstetrics and Gynecology, Graduate School of Medical Sciences, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-8582, Japan. Tel.: q81-92-642-5394; fax: q81-92-642-5414. E-mail address:
[email protected] ŽK. Okugawa.. 0020-7292r01r$20.00 䊚 2001 International Federation of Gynecology and Obstetrics. All rights reserved. PII: S 0 0 2 0 - 7 2 9 2 Ž 0 1 . 0 0 4 0 6 - 4
46
K. Okugawa et al. r International Journal of Gynecology & Obstetrics 74 (2001) 45᎐50
1. Introduction Correct preoperative diagnosis is essential to make an appropriate preoperative treatment plan in the management of ovarian tumors. Recently, the development of imaging techniques has increased the accuracy in diagnosing ovarian tumors. It is, however, difficult to give a precise preoperative diagnosis of the malignant potential of ovarian tumors. Therefore, detailed analysis of the clinical characteristics of ovarian tumors is required. Many clinicopathologic studies have been published to analyze the characteristics of ovarian cancers. However, little attention has been paid to benign ovarian tumors, despite the fact that they are one of the most common gynecological disorders. In this report, we performed a statistical analysis on the relationship between patients’ age, histological type, and the size of ovarian tumors in 1648 cases, in order to clarify their characteristics.
2. Materials and methods The data used in this study were taken from the clinical records of 1648 cases of histopathologically diagnosed ovarian tumors and tumor-like lesions treated at the Department of Obstetrics and Gynecology of Kyushu University Hospital, Fukuoka, Japan, from January 1981 to December 1995. Kyushu University Hospital is the main tertiary referral hospital in the Fukuoka medical area, with a female population of approximately one million. Classification of the histological diagnosis was based on the World Health Organization Histological Classification of Ovarian Tumors. For the purposes of analysis, tumor-like lesions were separated into two groups: endometriosis and others. We can be confident of the accuracy of the diagnoses since, at Kyushu University Hospital, all the routine pathological diagnoses made by general pathologists are reviewed at the weekly gynecologic oncology᎐pathology conference. In particular, all the malignant and LMP tumors, and tumors with rare pathology are thoroughly ex-
amined by a special group of pathologists who specialize in gynecologic pathology. Clinical information on patients was obtained from clinical records. Due to the fading of the ink on clinical records or a lack of detailed descriptions, information on patient age and tumor size was available in 1639 and 1499 cases, respectively. All the transabdominalrtransvaginal ultrasounds were done by clinical gynecologists as routine tumor investigation. Transvaginal ultrasounds have been utilized since around 1988 in this institution. Data were subjected to Kruskal᎐Wallis tests or Mann᎐Whitney U-tests, using the statistical software StatView 䊛 version 4.5 ŽAbacus Concepts Inc., Berkeley, USA.. The significance level was set at P- 0.05.
3. Results 3.1. Frequency of o¨ arian tumors and tumor-like lesions There were 840 Ž51%. cases of benign tumors, 73 Ž4%. cases of tumors of low malignant potential ŽLMP., 268 Ž16%. cases of malignant tumors and 467 Ž28%. cases of tumor-like lesions. The most common histological type among benign ovarian tumors was dermoid cyst Ž445 cases., followed by mucinous cystadenoma Ž162 cases. and serous cystadenoma Ž137 cases. ŽTable 1.. Dermoid cysts accounted for 53% Ž445r840 cases. of benign ovarian tumors and 38% Ž445r1181 cases. of all benign, LMP, or malignant tumors. On the other hand, serous cystadenoma accounted for 16% Ž137r840 cases. of benign ovarian tumors and 12% Ž137r1181 cases. of all benign, LMP, or malignant tumors. The other benign tumors included 33 cases of fibroma, 12 cases of theca cell tumor, 4 cases of Brenner tumor and mixed epithelial tumors that contained more than two histological types. The other LMP tumors included 2 cases of mixed epithelial tumor of low malignant potential and one proliferating Brenner tumor. The other malignant tumors included 29 cases of surface epithelial-stromal tumor other than four main subtypes of malignant tumors
K. Okugawa et al. r International Journal of Gynecology & Obstetrics 74 (2001) 45᎐50
47
Table 1 Number of cases in relation to the age and the histological type of ovarian tumors and tumor-like lesions Histological type
Tumor-like lesions
Mean age "S.D.a Žyears.
No. of cases in each age range Žyears. O 20
21᎐45
46᎐55
56᎐65
P 66
Unknown
Total no. of cases
Endometriosis Others
34.6" 8.1 35.0" 7.8 33.6" 8.7
6 4
288 112
37 14
0 2
0 0
3 1
467 334 133
Dermoid cyst Serous cystadenoma Mucinous cystadenoma Others
39.8" 16.4 35.0" 13.8 45.6" 17.5 43.9" 17.2 46.2" 17.3
32 7 9 5
334 71 82 47
36 19 26 12
21 14 24 16
19 24 21 16
3 2 0 0
840 445 137 162 96
Serous LMP Mucinous LMP Others
45.2" 18.3 37.9" 17.4 45.9" 18.3 60.0" 16.0
1 4 0
7 25 1
1 11 0
2 7 1
1 11 1
0 0 0
73 12 58 3
Serous ca.c Mucinous ca. Clear cell ca. Endometrioid ca. Others
51.9" 13.0 55.1" 10.8 52.0" 12.9 50.6" 9.9 51.1" 9.4 47.6" 17.3
0 0 0 0 5
17 10 12 10 24
36 8 19 13 13
26 7 8 4 16
18 5 3 4 10
0 0 0 0 0
268 97 30 42 31 68
40.5" 15.1
73
1040
245
148
133
9
1648
Benign tumors
LMPb tumors
Malignant tumors
Total a
Standard deviation. Tumors of low malignant potential. c Carcinoma. b
Žserous, mucinous, clear cell, and endometrioid., 15 cases of sex cord-stromal tumor, 23 cases of germ cell tumor and 1 malignant lymphoma. Metastatic tumors were excluded from this study. Among malignant tumors, clear cell carcinoma accounted for 16% Ž42r268 cases., whereas serous carcinoma accounted for 36% Ž97r268 cases.. 3.2. Relationship between the histological type and the age of the patients The age distribution of the patients and the histological type of the ovarian tumors are summarized in Table 1. The patients’ ages ranged from 9 to 92 years with a mean of 40.5 years and a median of 38 years. One thousand and forty patients Ž63%. were between the age of 21 and 45 years, 526 patients Ž32%. were more than 46
years old, and 73 patients Ž4%. were 20 years old or less. The age of the patients was significantly different among tumor-like lesions Žmean " S.D.s 34.6 " 8.1 years., benign tumors Ž39.8 " 16.4 years., LMP tumors Ž45.2" 18.3 years. and malignant tumors Ž51.9 " 13.0 years. Ž P - 0.0001.. Among serous tumors, serous cystadenomas Ž45.6 " 17.5 years. and serous LMP tumors Ž37.9" 17.4 years. were observed in significantly younger patients than serous carcinomas Ž55.1 " 10.8 years. Ž P- 0.0001 and 0.0013, respectively.. On the contrary, no significant difference was seen in the age of patients with LMP Ž45.9" 18.3 years. or malignant Ž52.0" 12.9 years. mucinous tumors. The number of cases of endometriosis and other tumor-like lesions peaked in the 21᎐45-years age group, and were rarely encountered in the post-
K. Okugawa et al. r International Journal of Gynecology & Obstetrics 74 (2001) 45᎐50
48
menopausal age group. Two tumor-like lesions seen in the range of 56 to 65 were both simple cysts, not otherwise specified. All of the three main subtypes of benign tumors Ždermoid, serous and mucinous. were most frequently encountered in patients of the 21᎐45-years age group. However, a substantial number of tumors were also seen in the older age group. The mean ages of the patients with tumor-like lesions Ž34.6" 8.1 years. or dermoid cysts Ž35.0" 13.8 years. were significantly lower than those with serous cystadenomas Ž45.6" 17.5 years. and mucinous cystadenomas Ž43.9" 17.2 years. Ž P- 0.0001.. Distribution of the age of patients with malignant and LMP tumors varied among histological subtypes. Patients with serous LMP tumors Ž37.9 " 17.4 years. were younger than those with other types of LMP tumors. The number of cases of
serous, clear cell and endometrioid carcinomas peaked in the 46᎐55-years age group, whereas cases of mucinous carcinomas peaked in patients of the 21᎐45-years age group. The ratio of serous carcinomas to all malignant tumors increased with age: 22% Ž17r78 cases. in the age range of 45 years or less; 45% Ž18r40 cases. in the range of 66 years or more. 3.3. Relationship between histological type and tumor size We analyzed the correlation between histological type and the maximum diameter of the tumors preoperatively measured by transabdominal andror transvaginal ultrasonography ŽTable 2.. The maximum diameter of the tumors was significantly different among tumor-like lesions Ž7.1
Table 2 Number of cases in relation to the size and the histological type of ovarian tumors and tumor-like lesions Histological type
7.1" 3.3 7.3" 3.2 6.4" 3.6
38 29
184 53
58 11
0 2
54 38
467 334 133
Dermoid cyst Serous cystadenoma Mucinous cystadenoma Others
10.9" 5.6 9.3" 4.1 10.4" 5.0 15.4" 7.1 12.1" 5.6
11 6 4 2
246 66 29 25
156 49 73 51
13 5 43 11
19 11 13 7
840 445 137 162 96
Serous LMP Mucinous LMP Others
18.5" 6.8 13.9" 6.1 19.6" 6.6 14.7" 6.1
0 1 0
3 1 1
6 28 1
2 28 1
1 0 0
73 12 58 3
Serous ca.c Mucinous ca. Clear cell ca. Endometrioid ca. Others
13.6" 6.5 10.4" 4.4 21.0" 8.0 15.4" 5.5 14.5" 5.8 13.0" 5.9
3 0 0 0 6
36 0 3 3 8
49 16 31 21 39
4 14 8 7 14
5 0 0 0 1
268 97 30 42 31 68
10.8" 6.0
100
658
589
152
149
1648
Benign tumors
LMPb tumors
Malignant tumors
Total Standard deviation. Tumors of low malignant potential. c Carcinoma.
10᎐19
P 20
Total no. of cases
5᎐9
Endometriosis Others
b
No. of cases in each size range Žcm. O4
Tumor-like lesions
a
Mean size "S.D.a Žcm.
Unknown
K. Okugawa et al. r International Journal of Gynecology & Obstetrics 74 (2001) 45᎐50
" 3.3 cm., benign tumors Ž10.9" 5.6 cm., malignant tumors Ž13.6" 6.5 cm. and LMP tumors Ž18.5" 6.8 cm. Ž P- 0.0001.. Among tumor-like lesions and the histological subtypes of benign tumors, the maximum diameter of mucinous cystadenoma Ž15.4" 7.1 cm. was significantly greater than that of any other subtype Ž Ps 0.0004.. Mucinous cystadenoma accounted for 58% Ž43r74 cases. of benign tumors and tumor-like lesions measuring 20 cm or more. The maximum diameter of malignant and LMP tumors most often ranged between 10 and 19 cm. However, it should be noted that nine of the malignant tumors and one of the LMP tumors were less than 4 cm in size.
4. Discussion The current study suggests that the overall distribution of the age of patients with ovarian tumors in Japan is very similar to that in western countries. In our study among Japanese women, 63% Ž1040r1639 cases. of ovarian tumors occurred in women between the ages of 21 and 45 years old, and 87% Ž1433r1639 cases. of them in women between 21 and 65 years old, while only 4% Ž73r1639 cases. occurred in women less than 20 years old. Scully et al. w1x described that approximately two-thirds of ovarian tumors occurred in women in the reproductive age group, and 80᎐90% of them in women between the ages of 20 and 65 years; well under 5% occurred in children. In this study of benign tumors, the most common histology was dermoid cyst. Katsube et al. w2x in their population-based histopathologic study of primary ovarian neoplasms in Colorado, USA, reported that the frequency of dermoid cysts was 26.5% and that of serous cystadenomas was 18.5%, with a dermoidrserous rate of 1.43. In our data, the frequencies of dermoid cysts and serous cystadenomas among primary ovarian neoplasms were 37.7% Ž445r1181 cases. and 11.6% Ž137r1181 cases., respectively, with a dermoidrserous rate of 3.25. Although our study is not a population-based study, these results suggest that dermoid cysts are more frequent and serous
49
cystadenomas are less frequent in Japan, when compared with the USA. Our results suggest that the incidence of clear cell carcinoma in Japan is higher compared to that in western countries; consistent with Jimbo et al. w3x. The prevalence of clear cell carcinoma among all epithelial ovarian carcinomas has been reported to be between 15.1 w4x and 17.8% w3x in Japan. In our study, clear cell carcinoma accounted for 16% of all malignant tumors of the ovary. However, it was reported that clear cell carcinoma accounted for only 3.9᎐6.0% of all ovarian cancers in western countries w5᎐8x. In this series, the median age of the patients with ovarian cancer was 52 years, whereas it was reported to be in the early 60s in the USA w9,10x. It is difficult to give a conclusive explanation for the difference in the median ages of patients with ovarian cancer between Japan and the USA, but differences in the histological distribution of ovarian malignancies may be one of the contributing factors. Race and environmental factors may also contribute to this difference. We found that tumor-like lesions are rare among postmenopausal women. There were only 2 cases of tumor-like lesions in patients over the age of 56 years, both of which were simple cysts with no obvious epithelial covering over the inner surface. It is suggested that ovarian tumors in postmenopausal women should be observed carefully as previously reported w5x, because ovarian tumors in postmenopausal women are mostly neoplastic. Our study showed that the mean maximum diameter was 7.1 cm in tumor-like lesions, 10.9 cm in benign tumors, 13.6 cm in malignant tumors, and 18.5 cm in LMP tumors. Koonings et al. w5x described the average size of benign ovarian tumors to be 8 = 10 cm, slightly smaller than that of malignant tumors Ž11 = 14 cm. and tumors of LMP Ž10 = 12 cm.. Rulin et al. w11x reported that 64% of adnexal masses greater than 10 cm in diameter were malignant, while only 1 out of 32 cases was malignant in the - 5-cm group among postmenopausal women. We analyzed the relationship between histological type, age distribution and tumor size of ovarian tumors in a group of Japanese patients. The
50
K. Okugawa et al. r International Journal of Gynecology & Obstetrics 74 (2001) 45᎐50
distribution of tumor histological type Žtumor-like lesions, benign, LMP, and malignant. was correlated against patient age and lesion diameter. As the mean age of patients increased and as the lesion diameter increased, the distribution of tumor type was found to change, with tumors in older patients or larger tumors more likely to be malignant. We also found that the frequency of some histologic subtypes, especially dermoid cysts and clear cell carcinomas may be high in Japan when compared with western countries. We understand, however, that approximately 9% of the information relating tumor size was unobtainable and these conclusions should be read with care. Further studies should be conducted to elucidate the epidemiologic and clinicopathologic characteristics of ovarian tumors in order to evaluate their malignant potentials.
w2x
w3x
w4x
w5x
w6x
w7x
Acknowledgments This study was supported in part by a Grant-inAid for Scientific Research ŽC. from the Ministry of Education, Science, Sports and Culture, Japan Žno. 12671612.. References w1x Scully RE, Young RH, Clement PB. In: Scully RE, Young RH, Clement PB, editors. Atlas of tumor pathology: tumor of the ovary, maldeveloped gonads,
w8x
w9x
w10x
w11x
fallopian tube, and broad ligament, 3rd ed. Washington, DC: Armed forces institute of pathology, 1998 27. Katsube Y, Berg JW, Silverberg SG. Epidemiologic pathology of ovarian tumors: a histopathologic review of primary ovarian neoplasms diagnosed in the Denver Standard Metropolitan Statistical Area, 1 July᎐31 December 1969 and 1 July᎐31 December 1979. Int J Gynecol Pathol 1982;1:3᎐16. Jimbo H, Yoshikawa H, Onda T, Yasugi T, Sakamoto A, Taketani Y. Prevalence of ovarian endometriosis in epithelial ovarian cancer. Int J Gynecol Obstet 1997;59: 245᎐250. Sakamoto A, Sasaki H, Furusato M, Suzuki M, Hirai Y, Tsugane S et al. Observer disagreement in histological classification of ovarian tumors in Japan. Gynecol Oncol 1994;54:54᎐58. Koonings PP, Campbell K, Mishell DR, Grimes DA. Relative frequency of primary ovarian neoplasms: a 10-year review. Obstet Gynecol 1989;74:921᎐926. Aure JC, Hoeg K, Kolstad P. Mesonephroid tumors of the ovary. Clinical and histopathologic studies. Obstet Gynecol 1971;37:860᎐867. Fine G, Clarke HD, Horn RC. Mesonephroma of the ovary. A clinical, morphological, and histogenetic appraisal. Cancer 1973;31:398᎐410. Kennedy AW, Biscotti CV, Hart WR, Webster KD. Ovarian clear cell adenocarcinoma. Gynecol Oncol 1989;32:342᎐349. ACOG. ACOG educational bulletin. Ovarian cancer. Number 250, August 1998 Žreplaces no. 141, May 1990.. Int J Gynecol Obstet 1998;63:301᎐310.. Yancik R. Ovarian cancer. Age contrasts in incidence, histology, disease stage at diagnosis, and mortality. Cancer 1993;71:517᎐523. Rulin MC, Preston AL. Adnexal masses in postmenopausal women. Obstet Gynecol 1987;70Ž4.:578᎐581.