Prevalence of Occult Malignancy in Patients Undergoing Hysterectomy for Benign Indications: 5-year Experience in a Tertiary Center

Öz

Hysterectomy is the most common gynecologic surgical procedure after cesarean section worldwide. The most common indication for hysterectomy is myoma uteri, but occult malignancies may be found in the final pathology results. In this article, we aimed to analyse the pathology results of patients who underwent hysterectomy with benign indication, to review the patients with occult malignancy in hysterectomy specimens and to discuss the issues to be considered in preoperative evaluation in the light of the literature. Data of 593 patients who underwent hysterectomy between 2017 - 2021 at Gaziosmanpaşa University, Department of Obstetrics and Gynecology were collected. Preoperative malignancy and postpartum hysterectomy were exclusion criteria. Indications for hysterectomy and the prevalence of occult malignancy were examined. Uterine myoma was the most common(40%) hysterectomy indication. Occult malignancy was detected in 7(1.2%) of 593 patients. Of the 7 patients with occult malignancy, 3 had sarcoma, 1 had cervical, 2 had ovarian and 1 had tubal cancer. Preoperative endometrial biopsies of patients who underwent hysterectomy due to leiomyoma and abnormal uterine bleeding were normal. Endometrial cancer was not encountered. Although there are no preoperative screening guidelines for uterine sarcoma and ovarian cancer, our study emphasized the need for careful preoperative evaluation especially for elderly patients even with benign indications. Developing sensitive methods for preoperative screening and diagnosis to reduce the incidence of occult cancer is required.

Anahtar Kelimeler

• Hysterectomy
• menometrorrhagia
• myoma uteri
• occult malignancy

Benign Endikasyonlarla Histerektomi Uygulanan Hastalarda Okült Malignensi Prevalansı: 3. Basamak Bir Hastanede 5 Yıllık Deneyim

Öz

Histerektomi, tüm dünyada sezaryen sonrası en sık uygulanan jinekolojik cerrahi prosedürdür. Histerektomi için en yaygın endikasyon myoma uteri'dir ancak nihai patoloji sonuçlarında okült maligniteler bulunabilir. Bu makalede, benign endikasyonla histerektomi yapılan hastaların patoloji sonuçlarını analiz etmeyi, histerektomi spesimenlerinde okült malignite saptanan hastaları gözden geçirmeyi ve preoperatif değerlendirmede dikkat edilmesi gereken konuları literatür ışığında tartışmayı amaçladık. Gaziosmanpaşa Üniversitesi Kadın Hastalıkları ve Doğum Anabilim Dalı'nda 2017 - 2021 yılları arasında histerektomi yapılan 593 hastanın verileri toplandı. Preoperatif malignite ve postpartum histerektomi dışlama kriterleriydi. Histerektomi endikasyonları ve okült malignite prevalansları incelendi. Uterin myom en sık(%40) histerektomi endikasyonuydu. Okült malignite 593 hastanın 7'sinde(%1,2) tespit edildi. Okült malignitesi olan 7 hastanın 3'ünde sarkom, 1'inde servikal, 2'sinde over ve 1'inde tubal kanser vardı. Leiomyom ve anormal uterin kanama nedeniyle histerektomi yapılan hastaların preoperatif endometriyal biyopsileri normaldi. Hiçbir hastada endometriyal kansere rastlanmadı. Uterin sarkom ve over kanseri için preoperatif tarama kılavuzları olmamasına rağmen, çalışmamız özellikle yaşlı hastalarda benign endikasyonlarda dahil olmak üzere dikkatli preoperatif değerlendirme yapılması gerektiğini vurguladı.

Anahtar Kelimeler

• Histerektomi
• menometroraji
• myoma uteri
• okült malignite

Kaynakça

1. 1. Annan JJ, Konney TO, Asubonteng GO, Awortwi WS. Two-year surgical review of elective hysterectomy for non-oncological indications: experience from a tertiary centre. International Journal of Reproduction, Contraception, Obstetrics and Gynecology. 2019;9(11):4404.
2. 2. Yilmaz EPT, Senocak GNC, Topdagi YE, Yildiz GA, Kumtepe Y. Incidence of occult malignancies identified during hysterectomies performed for benign indications. Journal of Gynecology Obstetrics and Human Reproduction. 2020;49(3):101620.
3. 3. Buderath P, Kimmig R, Dominowski L, Mach P. Hysterectomy in benign conditions: a 20-year single-center retrospective on the development of surgical techniques. Archives of Gynecology and Obstetrics. 2023;307(3):807-812.
4. 4. Learman LA, Kuppermann M, Gates E, Gregorich SE, Lewis J, Washington AE. Predictors of hysterectomy in women with common pelvic problems: a uterine survival analysis. Journal of the American College of Surgeons. 2007;204(4):633-641.
5. 5. Mahnert N, Morgan D, Campbell D, Johnston C, As-Sanie S. Unexpected gynecologic malignancy diagnosed after hysterectomy performed for benign indications. Obstetrics & Gynecology. 2015;125(2):397-405.
6. 6. Yuk J-S, Kim LY, Kim S-H, Lee JH. The incidence of unexpected uterine malignancy in women undergoing hysterectomy for a benign condition: a national population-Based study. Annals of surgical oncology. 2016;23:4029-4034.
7. 7. Desai VB, Wright JD, Gross CP, et al. Prevalence, characteristics, and risk factors of occult uterine cancer in presumed benign hysterectomy. American journal of obstetrics and gynecology. 2019;221(1):39. e31-39. e14.
8. 8. van den Haak L, de Kroon CD, Warmerdam MI, et al. Incidence and groups at risk for unexpected uterine leiomyosarcoma: a Dutch nationwide cohort study. Archives of Gynecology and Obstetrics. 2019;299:159-165.

9. 9. Wagner P, Kommoss F, Kommoss S, et al. Unexpected malignant uterine pathology: Incidence, characteristics and outcome in a large single-center series of hysterectomies for presumed benign uterine disease. Gynecologic oncology. 2019;153(1):49-54.
10. 10. Sandberg EM, Hehenkamp WJ, Geomini PM, Janssen PF, Jansen FW, Twijnstra AR. Laparoscopic hysterectomy for benign indications: clinical practice guideline. Archives of gynecology and obstetrics. 2017;296:597-606.
11. 11. Nurullayeva M. Benign endikasyonlarla histerektomi yapılan hastalarda preoperatif endometriyum örneklemesinin postoperatif premalign/malign patoloji sonuçlarla karşılaştırılması. 2020.
12. 12. Stock RJ, Kanbour A. Prehysterectomy curettage. Obstet Gynecol. May 1975;45(5):537-541.
13. 13. GotGSoGa O. Indication and technics of hysterectomy for benigne diseases. AWMF Registry No 015/077, March 2015. 2015.
14. 14. Wilcox LS, Koonin LM, Pokras R, Strauss LT, Xia Z, Peterson HB. Hysterectomy in the united states, 1988-1990. Obstetrics & Gynecology. 1994;83(4):549-555.
15. 15. Tazegül A. EvalatIon Of The ClInIcal And DemographIc CharacterIstIcs Of The Hysterectomy Cases Performed In Our ClInIc. Selcuk Medical Journal. 2010;26(1):19-22.
16. 16. Parker WH, Fu YS, Berek JSJO, Gynecology. Uterine sarcoma in patients operated on for presumed leiomyoma and rapidly growing leiomyoma. 1994;83(3):414-418.
17. 17. Nurullayeva M. Benign endikasyonlarla histerektomi yapılan hastalarda preoperatif endometriyum örneklemesinin postoperatif premalign/malign patoloji sonuçlarla karşılaştırılması, Ankara Yıldırım Beyazıt Üniversitesi Tıp Fakültesi; 2020.
18. 18. Gambone JC, Reiter RCJCO, Gynecology. Nonsurgical management of chronic pelvic pain: a multidisciplinary approach. 1990;33(1):205-211.
19. 19. Marcolin JC, Lichtenfels M, da Silva CA, de Farias CB. Gynecologic and breast cancers: what's new in chemoresistance and chemosensitivity tests? Current Problems in Cancer. 2023:100996.
20. 20. Parsons LHP, Pedersen R, Richardson DL, Kho KA. The prevalence of occult endometrial cancer in women undergoing hysterectomy for benign indications. European Journal of Obstetrics & Gynecology and Reproductive Biology. 2018;223:108-112.
21. 21. Lidor A, Ismajovich B, Confino E, David M. Histopathological findings in 226 women with post-menopausal uterine bleeding. Acta obstetricia et gynecologica Scandinavica. 1986;65(1):41-43.
22. 22. Alshdaifat EH, El-Deen Al-Horani SS, Al-Sous MM, Al-Horani S, Sahawneh FE, Sindiani AM. Histopathological pattern of endometrial biopsies in patients with abnormal uterine bleeding in a tertiary referral hospital in Jordan. Annals of Saudi Medicine. 2022;42(3):204-213.
23. 23. Ouldamer L, Rossard L, Arbion F, Marret H, Body G. Risk of incidental finding of endometrial cancer at the time of hysterectomy for benign condition. Journal of Minimally Invasive Gynecology. 2014;21(1):131-135.
24. 24. Belal S, Al-Sayed MA-W, Abd El Hamid HM, Hamed HM. Doppler Study of Uterine Artery and Ultrasonography of Endometrial Thickness in Perimenopausal and Postmenopausal Bleeding. Open Journal of Obstetrics and Gynecology. 2022;12(4):309-322.
25. 25. Lo KW, Yuen P. The role of outpatient diagnostic hysteroscopy in identifying anatomic pathology and histopathology in the endometrial cavity. The Journal of the American Association of Gynecologic Laparoscopists. 2000;7(3):381-385.
26. 26. Bakour SH, Khan KS, Gupta JK. Controlled analysis of factors associated with insufficient sample on outpatient endometrial biopsy. BJOG: An International Journal of Obstetrics & Gynaecology. 2000;107(10):1312-1314.
27. 27. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: a cancer journal for clinicians. 2018;68(6):394-424.
28. 28. Benoit AG, Krepart GV, Lotocki RJ. Results of prior cytologic screening in patients with a diagnosis of Stage I carcinoma of the cervix. American journal of obstetrics and gynecology. 1984;148(5):690-694.
29. 29. Chapman JA, Mannel RS, DiSaia PJ, Walker JL, Berman ML. Surgical treatment of unexpected invasive cervical cancer found at total hysterectomy. Obstetrics and gynecology. 1992;80(6):931-934.
30. 30. González-Martín A, Harter P, Leary A, et al. Newly diagnosed and relapsed epithelial ovarian cancer: ESMO Clinical Practice Guideline for diagnosis, treatment and follow-up☆. Annals of Oncology. 2023;34(10):833-848.
31. 31. Dodge JE, Covens AL, Lacchetti C, et al. Preoperative identification of a suspicious adnexal mass: a systematic review and meta-analysis. Gynecologic oncology. 2012;126(1):157-166.
32. 32. Van Calster B, Timmerman D, Bourne T, et al. Discrimination between benign and malignant adnexal masses by specialist ultrasound examination versus serum CA-125. JNCI: Journal of the National Cancer Institute. 2007;99(22):1706-1714.
33. 33. Poonyakanok V, Tanmahasamut P, Jaishuen A. Prospective comparative trial comparing O‐RADS, IOTA ADNEX model, and RMI score for preoperative evaluation of adnexal masses for prediction of ovarian cancer. Journal of Obstetrics and Gynaecology Research. 2023;49(5):1412-1417.
34. 34. Yang Y, Ju H, Huang Y. Diagnostic performance of IOTA SRand O-RADS combined with CA125, HE4, and risk of malignancy algorithm to distinguish benign and malignant adnexal masses. European Journal of Radiology.2023;165:110926.
35. 35. Forbes C, Fayter D, de Kock S, Quek RG. A systematic reviewof international guidelines and recommendations for the genetic screening, diagnosis, genetic counseling, and treatment of BRCA-mutated breast cancer. Cancer management andresearch. 2019:2321-2337.
36. 36. Byun JM, Cho HJ, Lee DS, et al. Frequency of serous tubalintraepithelial carcinoma (STIC) in patients with high grade serous ovarian cancer. Taiwanese Journal of Obstetrics andGynecology. 2023;62(1):107-111.
37. 37. Grossman DC, Curry SJ, Owens DK, et al. Screening forovarian cancer: US preventive services task forcerecommendation statement. Jama. 2018;319(6):588-594.
38. 38. Bostanci E, Ayas S, Gurbuz T, Gurbuz A, Karateke A.Retrospective analysis of 29 cases with uterine sarcoma: A single center experience. Dicle Medical Journal. 2015;42:175-180.
39. 39. George S, Barysauskas C, Serrano C, et al. Retrospective cohort study evaluating the impact of intraperitoneal morcellation on outcomes of localized uterine leiomyosarcoma. Cancer. 2014;120(20):3154-3158.
40. 40. Nishigaya Y, Kobayashi Y, Matsuzawa Y, et al. Diagnostic value of combination serum assay of lactate dehydrogenase, D‐dimer, and C‐reactive protein for uterine leiomyosarcoma. Journal of Obstetrics and Gynaecology Research.2019;45(1):189-194.
41. 41. Zhang F, Liu Y, Quan Q, Meng Y, Mu X. Diagnostic value ofpreoperative CA125, LDH and HE4 for leiomyosarcoma of the female reproductive system. Cancer Management andResearch. 2021:4657-4664.
42. 42. Skorstad M, Kent A, Lieng M. Uterine leiomyosarcoma–incidence, treatment, and the impact of morcellation. A nationwide cohort study. Acta obstetricia et gynecologicaScandinavica. 2016;95(9):984-990.
43. 43. Yilmaz N, Sahin I, Kilic S, Ozgu E, Gungor T, Bilge U.Assessment of the predictivity of preoperative serum CA 125 in the differential diagnosis of uterine leiomyoma and uterine sarcoma in the Turkish female population. Eur J Gynaecol Oncol. 2009;30(4):412-414.
44. 44. Tasaki A, Asatani MO, Umezu H, et al. Differential diagnosis of uterine smooth muscle tumors using diffusion-weighted imaging: correlations with the apparent diffusion coefficient and cell density. Abdominal imaging. 2015;40:1742-1752.
45. 45. Li HM, Liu J, Qiang JW, Zhang H, Zhang GF, Ma F.Diffusion-weighted imaging for differentiating uterine leiomyosarcoma from degenerated leiomyoma. Journal ofcomputer assisted tomography. 2017;41(4):599-606.
46. 46. Namimoto T, Yamashita Y, Awai K, et al. Combined use of T2-weighted and diffusion-weighted 3-T MR imaging fordifferentiating uterine sarcomas from benign leiomyomas.European radiology. 2009;19:2756-2764.
47. 47. Havrilesky LJ, Maxwell GL, Myers ER. Cost-effectiveness analysis of annual screening strategies for endometrial cancer. American journal of obstetrics and gynecology.2009;200(6):640. e641-640. e648.
48. 48. Bansal N, Herzog TJ, Burke W, Cohen CJ, Wright JD. Theutility of preoperative endometrial sampling for the detection of uterine sarcomas. Gynecologic oncology. 2008;110(1):43-48.
49. 49. Leibsohn S, d'Ablaing G, Mishell Jr DR, Schlaerth JB. Leiomyosarcoma in a series of hysterectomies performed forpresumed uterine leiomyomas. American journal of obstetricsand gynecology. 1990;162(4):968-976.
50. 50. Hinchcliff EM, Esselen KM, Watkins JC, et al. The role ofendometrial biopsy in the preoperative detection of uterine leiomyosarcoma. Journal of minimally invasive gynecology.2016;23(4):567-572.
51. 51. Skorstad M, Kent A, Lieng M. Preoperative evaluation in women with uterine leiomyosarcoma. A nationwide cohort study. Acta obstetricia et gynecologica Scandinavica.2016;95(11):1228-1234.
52. 52. Stovall T, Photopulos G, Poston W, Ling F, Sandles L. Pipelle endometrial sampling in patients with known endometrial carcinoma. International journal of gynecology & obstetrics.1992;38(2):147-148.
53. 53. Desai VB, Wright JD, Schwartz PE, et al. Occult gynecologic cancer in women undergoing hysterectomy or myomectomy for benign indications. Obstetrics & Gynecology. 2018;131(4):642-651.
54. 54. Żak K, Zaremba B, Rajtak A, Kotarski J, Amant F, Bobiński M. Preoperative differentiation of uterine leiomyomas and leiomyosarcomas: current possibilities and future directions. Cancers. 2022;14(8):1966.