Arch Gynecol Obstet DOI 10.1007/s00404-014-3611-z
CASE REPORT
Primary malignant mixed Mu¨llerian tumor of the fallopian tube after subtotal hysterectomy: A case report and literature review Jing Ji • Ping Zuo • Long Li • Yueling Wang
Received: 9 April 2014 / Accepted: 30 December 2014 Ó Springer-Verlag Berlin Heidelberg 2015
Introduction Malignant mixed Mu¨llerian tumors (MMMTs) are rare and highly aggressive neoplasms in the female genital tract which arise from Mu¨llerian-derived tissues. The most common site for MMMTs is the endometrium, followed by the ovaries, fallopian tubes, cervix, and vagina. Other extra-genital sites have also been reported, such as peritoneum, stomach, esophagus, colon, and spleen [1]. Primary MMMTs of the fallopian tube are extremely uncommon tumors, accounting for 0.1–0.5 % of all gynecologic malignancies [2]. There are only 81 cases of primary MMMTs reported in the literature [3]. We here report of a case of MMMT of the fallopian tube in a patient who had undergone a subtotal hysterectomy and unilateral adnexectomy 17 years ago, with a review of the literature.
Case report A 57-year-old Chinese female presented with complaints of intermittent lower abdominal pain and distention for 4 months. The medical history was significant for a subtotal hysterectomy and unilateral adnexectomy for a hysteromyoma 17 years ago. She also had anorexia and had a 6-kg weight loss. She had received inflammatory therapy for 2 weeks, but had no significant improvement in symptoms. A bimanual examination revealed a normal cervix, an absent
J. Ji P. Zuo L. Li Y. Wang (&) Department of Gynecology and Obstetrics, The First Affiliated Hospital of Medical School, Xi’an Jiaotong University Medical School, 277 West Yanta Road, Xi’an 710061, Shanxi, People’s Republic of China e-mail: [email protected]
uterus, and a large mass measuring 10.0 9 8 cm in the right pelvis. Transvaginal ultrasonography and pelvic CT showed a hypoechoic mass measuring 11.5 9 8.3 9 7.4 cm above the vaginal stump and pelvic ascites (Fig. 1). Laboratory tests revealed elevated serum levels of CA-125 (328.70 U/ ml), CA-199 (208.50 U/ml), CA-153 (70.11 U/ml), and a normal CEA level. The routine blood parameters, biochemistry tests, and a chest X-ray were within normal limits. 3 days after her physical examination, the patient underwent an exploratory laparotomy for the primary diagnosis of a malignant ovarian tumor. Approximately 1,800 ml of amber ascites was present, and the body of the uterus and the left fallopian tube and ovary were absent; the right fallopian was enlarged and adhered to the right ovary, which measured 12.0 9 10.0 9 10.0 cm. The ampulla of the right fallopian was approximately 2.5 cm in diameter. Several tubercles were scattered on the peritoneal surface and great omentum. Exploration of the upper abdomen was negative. The patient underwent a right salpingo-oophorectomy, omentectomy, appendectomy, pelvic lymph node dissection, and paraaortic lymph node biopsy. The final pathologic diagnosis was MMMT of the right fallopian tube with poorly differentiated adenocarcinoma and highly differentiated chondrosarcoma (Fig. 2). Immunohistochemical staining for CK7 and EMA were positive and CK20 was negative (carcinomatous component), while vimentin and S-100 were positive and SMA and DES were negative (sarcomatous component). The right ovary was metastasized by poorly differentiated adenocarcinoma, but the ascites, omentum, appendix, and pelvic and para-aortic lymph nodes were negative for malignant cells. The final clinicopathologic diagnosis was primary fallopian tube MMMT IIa (FIGO stage). Taking into account of the poor situation of the patient after surgery, we chose paclitaxel (175 mg/m2) and
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Arch Gynecol Obstet
Fig. 1 Transvaginal ultrasonography (a) and CT imaging (b). Transvaginal ultrasonography showing a large mass measuring 11.5 9 8.3 9 7.4 cm up the vaginal stump. CT imaging showing a
compound-density lesion measuring 7.5 9 7.6 9 9.9 cm can be seen in the abdomen and pelvic cavity, with a small amount of pelvic ascites
Fig. 2 Elements of the fimbrial MMMT. Poorly differentiated adenocarcinoma (a) and highly differentiated chondrosarcoma (b)
oxaliplatin (130 mg/m2) instead of carboplatin for the first combination chemotherapy. Then she received paclitaxel (175 mg/m2) and cisplatinum (75 mg/m2) for the last three cycles at 4-week intervals. One month post-operatively after the first cycle of chemotherapy, the serum CA-125 level declined to 12.70 U/ml. After four cycles of chemotherapy, the serum CA-125 level was 5.73 U/ml and abdominopelvic CT imaging showed no evidence of recurrence. Due to the poor family economic conditions, the patient gave up the follow-up treatment automatically. They chose traditional
123
Chinese medicine after they went home. So far, the patient has survived more than 16 months after the operation.
Discussion MMMTs are biphasic neoplasms composed of malignant epithelial and mesenchymal elements (carcinomatous and sarcomatous components). The carcinomatous components of MMMTs are usually serous, endometrioid, clear cell, or
Arch Gynecol Obstet
adenomatous. MMMTs are subdivided into homologous and heterologous tumors according to the sarcomatous components. In homologous tumors, both the carcinomatous and mesenchymal elements arise from normal components of the Mu¨llerian system, including fibrous tissue, endometrium, and smooth muscle. The sarcomatous elements of the heterologous tumors arise from the nonMu¨llerian system, such as skeletal muscle, bone, cartilage, or adipose tissue [4]. Primary MMMTs of the fallopian tube most often occur in postmenopausal women in the fifth or sixth decade of life at a mean age of 59.7 years [3]. The patient reported herein was 57 years of age, who underwent a subtotal hysterectomy and unilateral adnexectomy 17 years earlier. Most patients with MMMTs of the fallopian tube present with atypical bleeding, abdominal pain, and/or a pelvic mass, while patients with advanced disease may have urinary tract, gastrointestinal, or respiratory symptoms due to metastatic lesions. No specific tumor makers can successfully predict MMMT. The serum CA-125 can be elevated on occasion, but there is no evidence of a close relationship between CA-125 and MMMTs. It is difficult to differentiate MMMTs of the fallopian tube from ovarian cancer before surgery. Transvaginal ultrasonography, CT scanning, or MRI can help render a diagnosis, but lack specificity and accuracy; the diagnosis of fallopian tube MMMT is usually not made until the time of surgery and pathologic evaluation. The treatment approach for MMMT of the fallopian tube is similar to that of ovarian carcinoma. Surgical resection and platinum-based chemotherapy have been successfully used in the majority of patients [5]. Staging laparotomy should include collection of washings and/or ascites, a thorough exploration of all peritoneal surfaces, omentectomy, appendectomy, pelvic lymph node sampling, and peritoneal biopsies, as necessary. Aggressive cytoreductive surgery with removal of as much tumor as possible is warranted in patients with advanced disease. Adjuvant chemotherapy improves the prognosis. Because a diagnosis is difficult to establish in early-stage disease, and MMMTs are highly aggressive, the prognosis is usually very poor, with an average survival of 16.1 months [5]. In the current case, the patient underwent surgery for a hysteromyoma and only the right adnexa was preserved; the right fallopian tube MMMT was diagnosed 17 years later. There are no similar reports in the literature. The current case report raises the question of whether or not a prophylactic salpingectomy is indicated during a subtotal hysterectomy or total hysterectomy. There are two main controversial questions which need to be considered. First, would prophylactic salpingectomy cause earlier cystic degeneration of the remaining ovary? Second, would a prophylactic salpingectomy benefit the patient in
subsequent years compared to a hysterectomy alone? Most authorities believe that retaining normal fallopian tubes during a hysterectomy slows the degeneration of the ovary by preserving the blood vessels in the mesosalpinx, especially for perimenopausal women [6]. However, Morelli et al. [7] retrospectively compared 79 pairs of patients who underwent hysterectomies with or without bilateral salpingectomies and found that the patients in the prophylactic salpingectomy group had no negative effects in ovarian function by preserving blood vessel integrity in the proximity of the ovarian hilum and in the context of the mesosalpinx. In recent years, a number of studies have emerged supporting this point of view [8–10]. In contrast, a number of problems could arise years later in patients with conserved fallopian tubes, such as abdominal pain caused by a hydrosalpinx and tubo-ovarian cysts [11], prolapse of fallopian tubes [12], and although rare, ovarian and primary fallopian cancers [13], as in the patient reported herein. Some researchers believe that high-grade serous cancer of the ovary is derived from the epithelium of the fallopian tube, and most of the in situ carcinomas or intraepithelial precursors of cancers incidentally diagnosed are detected not in the ovary, but in the fimbrial portion of the fallopian tube [14, 15]. Therefore, prophylactic salpingectomy is a strategy which can be considered to decrease the risk of ovarian cancer. The British Columbia Ovarian Cancer Prevention Project [16] encourages prophylactic salpingectomy to reduce the long-term incidence of ovarian cancer. Morelli et al. [7] thought it would encourage prophylatic salpingectomy and estimated up to a 50 % reduction in ovarian cancer-related deaths 20 years after surgery. In conclusion, prophylactic salpingectomy in hysterectomy could reduce the incidence of post-operative complications, such as pelvic masses, and ovarian and primary fallopian cancers. As in the patient reported in our case, if she had accepted prophylactic salpingectomy 17 years ago, she would not have suffered the malignant fallopian tube cancer. However, an earlier cystic degeneration of the ovaries might occur; thus, we recommend ligating the mesosalpinx as close to the fallopian tube as possible to preserve the vessels supplying the orphan ovary. Conflict of interest
We declare that we have no conflict of interest.
References 1. Khanna SB, Dash K, Arora DS (2009) Malignant mixed mullerian tumor-case reports and review article. Apollo Med 6(3):227–241 2. Shen Y-M, Xie Y-P, Xu L, Yang K-X, Yu N, Yu Y, Wang J-H (2010) Malignant mixed mu¨llerian tumor of the fallopian tube: report of two cases and review of literature. Arch Gynecol Obstet 281(6):1023–1028
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Arch Gynecol Obstet 3. Gupta R, Jenison EL (2012) A rare case of carcinosarcoma of the fallopian tube presenting with torsion, rupture and hemoperitoneum. Gynecol Oncol Case Rep 2(1):4–5 4. D’Angelo E, Prat J (2011) Pathology of mixed mu¨llerian tumours. Best Pract Res Clin Obstet Gynaecol 25(6):705–718 5. Tsai C-P, Shih-Chu Ho E, Ke Y-M, Hsu S-T, Wang R-C, Lu C-H (2012) Stage III malignant mixed mu¨llerian tumor of the fallopian tube: a case of 5-year survival after optimal debulking and adjuvant chemotherapy with paclitaxel plus carboplatin. Taiwan J Obstet Gynecol 51(2):294–296 6. Ahn EH, Bai SW, Song CH, Kim JY, Jeong KA, Kim SK, Lee JS, Kwon JY, Park KH (2002) Effect of hysterectomy on conserved ovarian function. Yonsei Med J 43(1):53–58 7. Morelli M, Venturella R, Mocciaro R, Di Cello A, Rania E, Lico D, D’Alessandro P, Zullo F (2013) Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere. Gynecol Oncol 129:448–451 8. Nouh A, El Behery M, Alanwar A, Seleim B (2010) Total salpingectomy during abdominal hysterectomy preserves ovarian blood flow and function. WebmedCentral Obstet Gynaecol 1(9):WMC00707 9. Sezik M, Ozkaya O, Demir F, Sezik HT, Kaya H (2007) Total salpingectomy during abdominal hysterectomy: effects on
123
10.
11.
12. 13.
14.
15.
16.
ovarian reserve and ovarian stromal blood flow. J Obstet Gynaecol Res 33(6):863–869 Xi W, Gong F, Tang Y, Zhang H, Lu G (2012) Ovarian response to gonadotropins after laparoscopic salpingectomy for ectopic pregnancy. Int J Gynecol Obstet 116(2):93–96 Repasy I, Lendvai V, Koppan A, Bodis J, Koppan M (2009) Effect of the removal of the Fallopian tube during hysterectomy on ovarian survival: the orphan ovary syndrome. Eur J Obstet Gynecol Reprod Biol 144(1):64–67 Piacenza J, Salsano F (2001) Post-hysterectomy fallopian tube prolapse. Eur J Obstet Gynecol Reprod Biol 98(2):253–255 Warshal DP, Burgelson ER, Aikins JK, Rocereto TF (1999) Posthysterectomy fallopian tube carcinoma presenting with a positive Papanicolaou smear. Obstet Gynecol (5, Part 2) 94:834–836 Crum CP, Drapkin R, Kindelberger D, Medeiros F, Miron A, Lee Y (2007) Lessons from BRCA: the tubal fimbria emerges as an origin for pelvic serous cancer. Clin Med Res 5(1):35–44 Johannes D (2014) Revisiting the pathogenesis of ovarian cancer: the central role of the fallopian tube. Arch Gynecol Obstet 289:241–246 http://www.ovcare.ca/prevention/preventing_ovarian_cancer/. Accessed 1 Oct 2013
CASE REPORT
Primary malignant mixed Mu¨llerian tumor of the fallopian tube after subtotal hysterectomy: A case report and literature review Jing Ji • Ping Zuo • Long Li • Yueling Wang
Received: 9 April 2014 / Accepted: 30 December 2014 Ó Springer-Verlag Berlin Heidelberg 2015
Introduction Malignant mixed Mu¨llerian tumors (MMMTs) are rare and highly aggressive neoplasms in the female genital tract which arise from Mu¨llerian-derived tissues. The most common site for MMMTs is the endometrium, followed by the ovaries, fallopian tubes, cervix, and vagina. Other extra-genital sites have also been reported, such as peritoneum, stomach, esophagus, colon, and spleen [1]. Primary MMMTs of the fallopian tube are extremely uncommon tumors, accounting for 0.1–0.5 % of all gynecologic malignancies [2]. There are only 81 cases of primary MMMTs reported in the literature [3]. We here report of a case of MMMT of the fallopian tube in a patient who had undergone a subtotal hysterectomy and unilateral adnexectomy 17 years ago, with a review of the literature.
Case report A 57-year-old Chinese female presented with complaints of intermittent lower abdominal pain and distention for 4 months. The medical history was significant for a subtotal hysterectomy and unilateral adnexectomy for a hysteromyoma 17 years ago. She also had anorexia and had a 6-kg weight loss. She had received inflammatory therapy for 2 weeks, but had no significant improvement in symptoms. A bimanual examination revealed a normal cervix, an absent
J. Ji P. Zuo L. Li Y. Wang (&) Department of Gynecology and Obstetrics, The First Affiliated Hospital of Medical School, Xi’an Jiaotong University Medical School, 277 West Yanta Road, Xi’an 710061, Shanxi, People’s Republic of China e-mail: [email protected]
uterus, and a large mass measuring 10.0 9 8 cm in the right pelvis. Transvaginal ultrasonography and pelvic CT showed a hypoechoic mass measuring 11.5 9 8.3 9 7.4 cm above the vaginal stump and pelvic ascites (Fig. 1). Laboratory tests revealed elevated serum levels of CA-125 (328.70 U/ ml), CA-199 (208.50 U/ml), CA-153 (70.11 U/ml), and a normal CEA level. The routine blood parameters, biochemistry tests, and a chest X-ray were within normal limits. 3 days after her physical examination, the patient underwent an exploratory laparotomy for the primary diagnosis of a malignant ovarian tumor. Approximately 1,800 ml of amber ascites was present, and the body of the uterus and the left fallopian tube and ovary were absent; the right fallopian was enlarged and adhered to the right ovary, which measured 12.0 9 10.0 9 10.0 cm. The ampulla of the right fallopian was approximately 2.5 cm in diameter. Several tubercles were scattered on the peritoneal surface and great omentum. Exploration of the upper abdomen was negative. The patient underwent a right salpingo-oophorectomy, omentectomy, appendectomy, pelvic lymph node dissection, and paraaortic lymph node biopsy. The final pathologic diagnosis was MMMT of the right fallopian tube with poorly differentiated adenocarcinoma and highly differentiated chondrosarcoma (Fig. 2). Immunohistochemical staining for CK7 and EMA were positive and CK20 was negative (carcinomatous component), while vimentin and S-100 were positive and SMA and DES were negative (sarcomatous component). The right ovary was metastasized by poorly differentiated adenocarcinoma, but the ascites, omentum, appendix, and pelvic and para-aortic lymph nodes were negative for malignant cells. The final clinicopathologic diagnosis was primary fallopian tube MMMT IIa (FIGO stage). Taking into account of the poor situation of the patient after surgery, we chose paclitaxel (175 mg/m2) and
123
Arch Gynecol Obstet
Fig. 1 Transvaginal ultrasonography (a) and CT imaging (b). Transvaginal ultrasonography showing a large mass measuring 11.5 9 8.3 9 7.4 cm up the vaginal stump. CT imaging showing a
compound-density lesion measuring 7.5 9 7.6 9 9.9 cm can be seen in the abdomen and pelvic cavity, with a small amount of pelvic ascites
Fig. 2 Elements of the fimbrial MMMT. Poorly differentiated adenocarcinoma (a) and highly differentiated chondrosarcoma (b)
oxaliplatin (130 mg/m2) instead of carboplatin for the first combination chemotherapy. Then she received paclitaxel (175 mg/m2) and cisplatinum (75 mg/m2) for the last three cycles at 4-week intervals. One month post-operatively after the first cycle of chemotherapy, the serum CA-125 level declined to 12.70 U/ml. After four cycles of chemotherapy, the serum CA-125 level was 5.73 U/ml and abdominopelvic CT imaging showed no evidence of recurrence. Due to the poor family economic conditions, the patient gave up the follow-up treatment automatically. They chose traditional
123
Chinese medicine after they went home. So far, the patient has survived more than 16 months after the operation.
Discussion MMMTs are biphasic neoplasms composed of malignant epithelial and mesenchymal elements (carcinomatous and sarcomatous components). The carcinomatous components of MMMTs are usually serous, endometrioid, clear cell, or
Arch Gynecol Obstet
adenomatous. MMMTs are subdivided into homologous and heterologous tumors according to the sarcomatous components. In homologous tumors, both the carcinomatous and mesenchymal elements arise from normal components of the Mu¨llerian system, including fibrous tissue, endometrium, and smooth muscle. The sarcomatous elements of the heterologous tumors arise from the nonMu¨llerian system, such as skeletal muscle, bone, cartilage, or adipose tissue [4]. Primary MMMTs of the fallopian tube most often occur in postmenopausal women in the fifth or sixth decade of life at a mean age of 59.7 years [3]. The patient reported herein was 57 years of age, who underwent a subtotal hysterectomy and unilateral adnexectomy 17 years earlier. Most patients with MMMTs of the fallopian tube present with atypical bleeding, abdominal pain, and/or a pelvic mass, while patients with advanced disease may have urinary tract, gastrointestinal, or respiratory symptoms due to metastatic lesions. No specific tumor makers can successfully predict MMMT. The serum CA-125 can be elevated on occasion, but there is no evidence of a close relationship between CA-125 and MMMTs. It is difficult to differentiate MMMTs of the fallopian tube from ovarian cancer before surgery. Transvaginal ultrasonography, CT scanning, or MRI can help render a diagnosis, but lack specificity and accuracy; the diagnosis of fallopian tube MMMT is usually not made until the time of surgery and pathologic evaluation. The treatment approach for MMMT of the fallopian tube is similar to that of ovarian carcinoma. Surgical resection and platinum-based chemotherapy have been successfully used in the majority of patients [5]. Staging laparotomy should include collection of washings and/or ascites, a thorough exploration of all peritoneal surfaces, omentectomy, appendectomy, pelvic lymph node sampling, and peritoneal biopsies, as necessary. Aggressive cytoreductive surgery with removal of as much tumor as possible is warranted in patients with advanced disease. Adjuvant chemotherapy improves the prognosis. Because a diagnosis is difficult to establish in early-stage disease, and MMMTs are highly aggressive, the prognosis is usually very poor, with an average survival of 16.1 months [5]. In the current case, the patient underwent surgery for a hysteromyoma and only the right adnexa was preserved; the right fallopian tube MMMT was diagnosed 17 years later. There are no similar reports in the literature. The current case report raises the question of whether or not a prophylactic salpingectomy is indicated during a subtotal hysterectomy or total hysterectomy. There are two main controversial questions which need to be considered. First, would prophylactic salpingectomy cause earlier cystic degeneration of the remaining ovary? Second, would a prophylactic salpingectomy benefit the patient in
subsequent years compared to a hysterectomy alone? Most authorities believe that retaining normal fallopian tubes during a hysterectomy slows the degeneration of the ovary by preserving the blood vessels in the mesosalpinx, especially for perimenopausal women [6]. However, Morelli et al. [7] retrospectively compared 79 pairs of patients who underwent hysterectomies with or without bilateral salpingectomies and found that the patients in the prophylactic salpingectomy group had no negative effects in ovarian function by preserving blood vessel integrity in the proximity of the ovarian hilum and in the context of the mesosalpinx. In recent years, a number of studies have emerged supporting this point of view [8–10]. In contrast, a number of problems could arise years later in patients with conserved fallopian tubes, such as abdominal pain caused by a hydrosalpinx and tubo-ovarian cysts [11], prolapse of fallopian tubes [12], and although rare, ovarian and primary fallopian cancers [13], as in the patient reported herein. Some researchers believe that high-grade serous cancer of the ovary is derived from the epithelium of the fallopian tube, and most of the in situ carcinomas or intraepithelial precursors of cancers incidentally diagnosed are detected not in the ovary, but in the fimbrial portion of the fallopian tube [14, 15]. Therefore, prophylactic salpingectomy is a strategy which can be considered to decrease the risk of ovarian cancer. The British Columbia Ovarian Cancer Prevention Project [16] encourages prophylactic salpingectomy to reduce the long-term incidence of ovarian cancer. Morelli et al. [7] thought it would encourage prophylatic salpingectomy and estimated up to a 50 % reduction in ovarian cancer-related deaths 20 years after surgery. In conclusion, prophylactic salpingectomy in hysterectomy could reduce the incidence of post-operative complications, such as pelvic masses, and ovarian and primary fallopian cancers. As in the patient reported in our case, if she had accepted prophylactic salpingectomy 17 years ago, she would not have suffered the malignant fallopian tube cancer. However, an earlier cystic degeneration of the ovaries might occur; thus, we recommend ligating the mesosalpinx as close to the fallopian tube as possible to preserve the vessels supplying the orphan ovary. Conflict of interest
We declare that we have no conflict of interest.
References 1. Khanna SB, Dash K, Arora DS (2009) Malignant mixed mullerian tumor-case reports and review article. Apollo Med 6(3):227–241 2. Shen Y-M, Xie Y-P, Xu L, Yang K-X, Yu N, Yu Y, Wang J-H (2010) Malignant mixed mu¨llerian tumor of the fallopian tube: report of two cases and review of literature. Arch Gynecol Obstet 281(6):1023–1028
123
Arch Gynecol Obstet 3. Gupta R, Jenison EL (2012) A rare case of carcinosarcoma of the fallopian tube presenting with torsion, rupture and hemoperitoneum. Gynecol Oncol Case Rep 2(1):4–5 4. D’Angelo E, Prat J (2011) Pathology of mixed mu¨llerian tumours. Best Pract Res Clin Obstet Gynaecol 25(6):705–718 5. Tsai C-P, Shih-Chu Ho E, Ke Y-M, Hsu S-T, Wang R-C, Lu C-H (2012) Stage III malignant mixed mu¨llerian tumor of the fallopian tube: a case of 5-year survival after optimal debulking and adjuvant chemotherapy with paclitaxel plus carboplatin. Taiwan J Obstet Gynecol 51(2):294–296 6. Ahn EH, Bai SW, Song CH, Kim JY, Jeong KA, Kim SK, Lee JS, Kwon JY, Park KH (2002) Effect of hysterectomy on conserved ovarian function. Yonsei Med J 43(1):53–58 7. Morelli M, Venturella R, Mocciaro R, Di Cello A, Rania E, Lico D, D’Alessandro P, Zullo F (2013) Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere. Gynecol Oncol 129:448–451 8. Nouh A, El Behery M, Alanwar A, Seleim B (2010) Total salpingectomy during abdominal hysterectomy preserves ovarian blood flow and function. WebmedCentral Obstet Gynaecol 1(9):WMC00707 9. Sezik M, Ozkaya O, Demir F, Sezik HT, Kaya H (2007) Total salpingectomy during abdominal hysterectomy: effects on
123
10.
11.
12. 13.
14.
15.
16.
ovarian reserve and ovarian stromal blood flow. J Obstet Gynaecol Res 33(6):863–869 Xi W, Gong F, Tang Y, Zhang H, Lu G (2012) Ovarian response to gonadotropins after laparoscopic salpingectomy for ectopic pregnancy. Int J Gynecol Obstet 116(2):93–96 Repasy I, Lendvai V, Koppan A, Bodis J, Koppan M (2009) Effect of the removal of the Fallopian tube during hysterectomy on ovarian survival: the orphan ovary syndrome. Eur J Obstet Gynecol Reprod Biol 144(1):64–67 Piacenza J, Salsano F (2001) Post-hysterectomy fallopian tube prolapse. Eur J Obstet Gynecol Reprod Biol 98(2):253–255 Warshal DP, Burgelson ER, Aikins JK, Rocereto TF (1999) Posthysterectomy fallopian tube carcinoma presenting with a positive Papanicolaou smear. Obstet Gynecol (5, Part 2) 94:834–836 Crum CP, Drapkin R, Kindelberger D, Medeiros F, Miron A, Lee Y (2007) Lessons from BRCA: the tubal fimbria emerges as an origin for pelvic serous cancer. Clin Med Res 5(1):35–44 Johannes D (2014) Revisiting the pathogenesis of ovarian cancer: the central role of the fallopian tube. Arch Gynecol Obstet 289:241–246 http://www.ovcare.ca/prevention/preventing_ovarian_cancer/. Accessed 1 Oct 2013
