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doi:10.1111/jog.12458
J. Obstet. Gynaecol. Res. Vol. 40, No. 10: 2114–2117, October 2014
Bilateral tubal and intrauterine pregnancies diagnosed at laparoscopy Takanori Fukuda, Hiromi Inoue, Yuina Toyama, Tomoyuki Ichida, Yoshie Uzawa, Mika Monma, Tsuyoshi Kusaka and Yutaka Kohata Department of Obstetrics and Gynecology, Shonan Kamakura General Hospital, Kamakura City, Japan
Abstract A 32-year-old woman had bilateral tubal and intrauterine pregnancies after hyperovulation with clomiphene citrate and subsequent artificial insemination with husband’s semen. Laparoscopic surgery revealed bilateral tubal pregnancies. Salpingectomy was performed on the left tube and linear salpingotomy was performed on the right tube. The postoperative course was uneventful. The patient delivered a healthy girl vaginally at 39 weeks’ gestation. Only eight cases with bilateral and intrauterine pregnancy have been reported. The live birth rate of bilateral tubal pregnancy and intrauterine pregnancy is 60% (6/10), which is similar to that of heterotopic pregnancy. Laparoscopic surgery is effective for confirming the diagnosis and treating heterotopic pregnancy. Key words: bilateral tubal pregnancy, heterotopic pregnancy, laparoscopic surgery.
Introduction The incidence of natural heterotopic pregnancy is approximately 1/30 000 pregnancies.1 There has been a recent tendency for the incidence of heterotopic pregnancy to increase owing to the increased incidence of pelvic inflammatory disease and assisted reproductive techniques (ART). Bilateral tubal pregnancy co-existing with intrauterine pregnancy is very rare, with only eight case reports being reported so far. Most cases have been caused by gonadotrophin or ART.
Case Report The patient was a 32-year-old woman (gravida 1, para 0) with no history of pelvic inflammation or prior surgery and no family history. She had a history of ovulatory disturbance, and clomiphene citrate (100 mg/day for 5 days) had been prescribed for the prior 6 months. Artificial insemination with the husband’s semen after ovulation with clomiphene citrate
and human chorionic gonadotrophin (hCG) injection had been performed by a gynecologic clinic. An intrauterine gestational sac was identified at 5 weeks’ gestation. She visited our hospital with the chief complaint of intermittent pain at 6 weeks’ gestation. Vaginal sonography revealed an intrauterine sac containing a fetus, left adnexal mass of 5 cm in diameter and a trace of fluid in the pelvic cavity. Initially, ovarian bleeding was considered. We decided to follow her up as an outpatient. No remarkable change in the left adnexal mass was observed by weekly sonography. At 9 weeks’ gestation, she had continuous abdominal pain and minor genital bleeding. Vaginal sonography revealed that the left adnexal mass had enlarged to 9 cm in diameter (Fig. 1) and blood had further accumulated in the pelvic cavity. Serum β-hCG was 165 395 mIU/mL. Chlamydia antibody test was negative. She was admitted and a diagnostic laparoscopy was performed with the suspicion of a possible heterotopic pregnancy. Laparoscopic surgery revealed about 500 mL of hemoperitoneum and a left hematosalpinx and salpingectomy was performed on the left tube (Fig. 2).
Received: April 25 2013. Accepted: March 21 2014. Reprint request to: Dr Takanori Fukuda, Shonandai 2-38-1 Fujisawa City, Kanagawa 252-0804, Japan. Email: [email protected]; [email protected]
2114
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
Heterotopic pregnancy
Figure 1 Vaginal sonography showing left adnexal mass.
Figure 3 Right ampullary tubal pregnancy.
Figure 2 Swelled left tubal mass.
Enlargement of the other fallopian tube was identified and linear salpingotomy was performed on a right tubal pregnancy (Fig. 3). The postoperative course was uneventful. The pathologic examination confirmed villi in both fallopian tubes. The intrauterine pregnancy continued with no complication and she vaginally delivered a healthy normal-weight girl at 39 weeks’ gestation.
Discussion Bilateral tubal pregnancy co-existing with intrauterine pregnancy is very rare (Table 1).2–10 In all except one case, induction of ovulation or ART was performed. In seven cases, laparoscopic surgery was performed. In
one case, diagnosis was made in only lateral tubal pregnancy and laparotomy was performed 1 week later. In just three cases, correct diagnosis was made by sonography. In one case it was managed expectantly. Heterotopic pregnancy is twice as likely as intrauterine-only pregnancy to end in spontaneous abortion. There is no difference in perinatal outcomes between heterotopic and intrauterine-only pregnancy progressing to live birth.11 The live birth rate of heterotopic pregnancy is 58.3% in the same report. The live birth rate of bilateral tubal pregnancy and intrauterine pregnancy is 60% (6/10), which is similar to that of heterotopic pregnancy. Although heterotopic pregnancy is considered, when the serum hCG level is higher than expected for gestational age, the diagnosis of heterotopic pregnancy is difficult. Diagnosis of bilateral tubal pregnancy co-existing with intrauterine pregnancy is even more difficult. It has been reported that magnetic resonance imaging (MRI) is an effective modality for diagnosing ectopic pregnancy.12 MRI was not performed because of the risk of organogenesis in this case. Surgery is needed to confirm the diagnosis. Laparoscopic surgery is less invasive and effective for diagnosis and treatment. Linear salpingotomy was performed for the following reasons: no diagnosis of contralateral tubal pregnancy was made before surgery; we were unable to obtain consent from the patient for bilateral salpingectomy as this would have resulted in loss of the ability to conceive naturally after the current pregnancy, and preservation of the fallopian tube was
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
2115
2116
30
35
31
29
38
39
28
32
34
32
Hanf 2
Dietz3
Jonler4
Wang5
Pan6
Hoopmann7
Bettocchi8
Nikolic9
Jeong10
This case
G1P0
G3P2
G2P1
G2P0
G0P0
G3P1
G0P0
G0P0
G2P2
G1P0
Parity
10
8
10
7
6
7
4
6
6
7
Gestational week
Clomiphene+AIH
Clomiphene
None
Gonadotrophin
ICSI
IVF-ET
GIFT
IVF-ET
Gonadotrophin
IVF-ET
Treatment for infertility
NA
NA
NA
NA
3
3
3
Unknown
NA
5
Number of ET
1
1
1
5
1
1
2
1
3
1
Intrauterine sac (n)
38 weeks cesarean section
Outcome
Laparoscopic bilateral salpingectomy D&C Laparoscopic salpingectomy+salpingotomy
Bilateral salpingectomy
Laparoscopic bilateral salpingostomy D&C Laparoscopic salpingectomy+salpingotomy
Bilateral salpingectomy
39 weeks normal vaginal delivery
Miscarriage
39 weeks normal vaginal delivery
Term twins after selective reduction
Miscarriage
Term normal vaginal delivery
Laparoscopic Miscarriage salpingectomy Salpingo-oophorectomy D&C Abortion Laparoscopic bilateral salpingotomy Expectant management 37 weeks twins cesarean section
Laparoscopic bilateral salpingectomy
Operation
AIH, artificial insemination with the husband’s semen; D&C, dilatation and curettage; ET, embryo transfer; GIFT, gamete intrafallopian transfer; ICSI, intracytoplasmic sperm injection; IVF, in vitro fertilization; NA, not applicable.
Age (years)
Author
Table 1 Case of bilateral tubal pregnancy and intrauterine pregnancies
T. Fukuda et al.
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
Heterotopic pregnancy
determined to be possible because the right tubal pregnancy site was small and had not ruptured. The possibility of persistent ectopic pregnancy might have remained after linear salpingotomy, and we thus carefully performed the procedure to leave no residual portion. In the previous case, a similar surgical procedure had also resulted in a full-term intrauterine pregnancy.8 In persistent ectopic pregnancy cases with hemoperitoneum, our intention is to repeat surgery. In vitro fertilization (IVF) has been improved to lower risks without compromising pregnancy rate. Cancellation of insemination or cryopreservation of excess embryos after IVF and increased use of elective singleembryo transfer can reduce multiple pregnancy.13 Frozen-thawed embryo transfer can reduce the incidence of ectopic pregnancy.14 It would thus seem that artificial insemination with the husband’s semen with ovarian stimulation is in effect the leading contributor to multiple births.15 In fact, recent reports indicate that the leading contributor is hyperovulation due to fertility drugs rather than IVF. In the past, there was a case in which a contralateral tubal pregnancy was detected during the postoperative period, leading to repeat surgery.3 When surgery is performed for patients diagnosed with ectopic pregnancy after the use of fertility drugs, surgeons need to thoroughly examine whether there is any other pregnancy site, including the contralateral fallopian tube. Above all, controlled ovarian stimulation is important to prevent multiple or heterotopic pregnancy.
Disclosure
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
None declared. 14.
References 1. Duce MN, Ozer C, Egilmez H, Apaydin FD, Yildiz A, Kara E. Heterotopic pregnancy: Case report. Abdo Imaging 2002; 27: 677–679. 2. Hanf V, Dietl J, Gagsteiger F, Pfeiffer KH. Bilateral tubal pregnancy with intra-uterine gestation after IVF-ET: Therapy
15.
by bilateral laparoscopic salpingectomy; a case report. Eur J Obstet Gynecol Reprod Biol 1990; 37: 87–90. Dietz TU, Haenggi W, Birkhaeuser M, Gyr T, Dreher E. Combined bilateral tubal and multiple intrauterine pregnancy after ovulation induction. Eur J Obstet Gynecol Reprod Biol 1993; 48: 69–71. Jonler M, Rasmussen KL, Lundoorff P. Coexistence of bilateral tubal and intrauterine pregnancy. Acta Obstet Gynecol Scand 1995; 74: 750–752. Wang YL, Yang TS, Chang SP, Ng HT. Heterotopic pregnancy after GIFT managed with expectancy: A case report. Chin Med J 1996; 58: 218–222. Pan HS, Chuang J, Chiu SF et al. Heterotopic triplet pregnancy: Report of a case with bilateral tubal pregnancy and an intrauterine pregnancy. Hum Reprod 2002; 17: 1363–1366. Hoopmann M, Wilhelm L, Possover M, Nawroth F. Heterotopic triplet pregnancy with bilateral tubal and intrauterine pregnancy after IVF. Reprod Biomed Online 2003; 6: 345–348. Bettocchi S, Nappi L, Ceci O et al. Simultaneous bilateral tubal pregnancies and intrauterine pregnancy with five fetuses. J Am Assoc Gynecol Laparosc 2004; 11: 195–196. Jeong HC, Park IH, Yoon YS et al. Heterotopic triplet pregnancy with bilateral tubal and intrauterine pregnancy after spontaneous conception. Eur J Obstet Gynecol Reprod Biol 2009; 142: 161–162. Nikolic B, Mitrovic A, Pavlovic DV, Cirovic DM, Dragojevic-Dikic S, Lukic R. Triple pregnancy: Intrauterine and bilateral tubal ectopic pregnancies. Aust N Z J Obstet Gynaecol 2004; 44: 260–261. Clayton HB, Schieve LA, Peterson HB, Jamieson DJ, Reynolds MA, Wright VC. A comparison of heterotopic and intrauterine-only pregnancy outcomes after assisted reproductive technologies in the United States from 1999 to 2002. Fertil Steril 2007; 71: 303–309. Takahashi A, Takahama J, Marugami N et al. Ectopic pregnancy: MRI findings and clinical utility. Abdom Imaging 2013; 38: 844–850. Stillman RJ, Richter KS, Banks NK, Graham JR. Elective single embryo transfer: A 6-year progressive implementation of 784 single blastocyst transfers and the influence of payment method on patient choice. Fertil Steril 2009; 92: 1895– 1906. Shapiro BS, Daneshmand ST, De Leon L, Garmer FC, Aguirre M, Hudson C. Frozen-thawed embryo transfer is associated with a significantly reduced incidence of ectopic pregnancy. Fertil Steril 2012; 98: 1490–1494. McClamrock HD, Jones HW Jr, Adashi EY. Ovarian stimulation and intrauterine insemination at the quarter centennial: Implications for the multiple births epidemic. Fertil Steril 2012; 97: 802–809.
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
2117
doi:10.1111/jog.12458
J. Obstet. Gynaecol. Res. Vol. 40, No. 10: 2114–2117, October 2014
Bilateral tubal and intrauterine pregnancies diagnosed at laparoscopy Takanori Fukuda, Hiromi Inoue, Yuina Toyama, Tomoyuki Ichida, Yoshie Uzawa, Mika Monma, Tsuyoshi Kusaka and Yutaka Kohata Department of Obstetrics and Gynecology, Shonan Kamakura General Hospital, Kamakura City, Japan
Abstract A 32-year-old woman had bilateral tubal and intrauterine pregnancies after hyperovulation with clomiphene citrate and subsequent artificial insemination with husband’s semen. Laparoscopic surgery revealed bilateral tubal pregnancies. Salpingectomy was performed on the left tube and linear salpingotomy was performed on the right tube. The postoperative course was uneventful. The patient delivered a healthy girl vaginally at 39 weeks’ gestation. Only eight cases with bilateral and intrauterine pregnancy have been reported. The live birth rate of bilateral tubal pregnancy and intrauterine pregnancy is 60% (6/10), which is similar to that of heterotopic pregnancy. Laparoscopic surgery is effective for confirming the diagnosis and treating heterotopic pregnancy. Key words: bilateral tubal pregnancy, heterotopic pregnancy, laparoscopic surgery.
Introduction The incidence of natural heterotopic pregnancy is approximately 1/30 000 pregnancies.1 There has been a recent tendency for the incidence of heterotopic pregnancy to increase owing to the increased incidence of pelvic inflammatory disease and assisted reproductive techniques (ART). Bilateral tubal pregnancy co-existing with intrauterine pregnancy is very rare, with only eight case reports being reported so far. Most cases have been caused by gonadotrophin or ART.
Case Report The patient was a 32-year-old woman (gravida 1, para 0) with no history of pelvic inflammation or prior surgery and no family history. She had a history of ovulatory disturbance, and clomiphene citrate (100 mg/day for 5 days) had been prescribed for the prior 6 months. Artificial insemination with the husband’s semen after ovulation with clomiphene citrate
and human chorionic gonadotrophin (hCG) injection had been performed by a gynecologic clinic. An intrauterine gestational sac was identified at 5 weeks’ gestation. She visited our hospital with the chief complaint of intermittent pain at 6 weeks’ gestation. Vaginal sonography revealed an intrauterine sac containing a fetus, left adnexal mass of 5 cm in diameter and a trace of fluid in the pelvic cavity. Initially, ovarian bleeding was considered. We decided to follow her up as an outpatient. No remarkable change in the left adnexal mass was observed by weekly sonography. At 9 weeks’ gestation, she had continuous abdominal pain and minor genital bleeding. Vaginal sonography revealed that the left adnexal mass had enlarged to 9 cm in diameter (Fig. 1) and blood had further accumulated in the pelvic cavity. Serum β-hCG was 165 395 mIU/mL. Chlamydia antibody test was negative. She was admitted and a diagnostic laparoscopy was performed with the suspicion of a possible heterotopic pregnancy. Laparoscopic surgery revealed about 500 mL of hemoperitoneum and a left hematosalpinx and salpingectomy was performed on the left tube (Fig. 2).
Received: April 25 2013. Accepted: March 21 2014. Reprint request to: Dr Takanori Fukuda, Shonandai 2-38-1 Fujisawa City, Kanagawa 252-0804, Japan. Email: [email protected]; [email protected]
2114
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
Heterotopic pregnancy
Figure 1 Vaginal sonography showing left adnexal mass.
Figure 3 Right ampullary tubal pregnancy.
Figure 2 Swelled left tubal mass.
Enlargement of the other fallopian tube was identified and linear salpingotomy was performed on a right tubal pregnancy (Fig. 3). The postoperative course was uneventful. The pathologic examination confirmed villi in both fallopian tubes. The intrauterine pregnancy continued with no complication and she vaginally delivered a healthy normal-weight girl at 39 weeks’ gestation.
Discussion Bilateral tubal pregnancy co-existing with intrauterine pregnancy is very rare (Table 1).2–10 In all except one case, induction of ovulation or ART was performed. In seven cases, laparoscopic surgery was performed. In
one case, diagnosis was made in only lateral tubal pregnancy and laparotomy was performed 1 week later. In just three cases, correct diagnosis was made by sonography. In one case it was managed expectantly. Heterotopic pregnancy is twice as likely as intrauterine-only pregnancy to end in spontaneous abortion. There is no difference in perinatal outcomes between heterotopic and intrauterine-only pregnancy progressing to live birth.11 The live birth rate of heterotopic pregnancy is 58.3% in the same report. The live birth rate of bilateral tubal pregnancy and intrauterine pregnancy is 60% (6/10), which is similar to that of heterotopic pregnancy. Although heterotopic pregnancy is considered, when the serum hCG level is higher than expected for gestational age, the diagnosis of heterotopic pregnancy is difficult. Diagnosis of bilateral tubal pregnancy co-existing with intrauterine pregnancy is even more difficult. It has been reported that magnetic resonance imaging (MRI) is an effective modality for diagnosing ectopic pregnancy.12 MRI was not performed because of the risk of organogenesis in this case. Surgery is needed to confirm the diagnosis. Laparoscopic surgery is less invasive and effective for diagnosis and treatment. Linear salpingotomy was performed for the following reasons: no diagnosis of contralateral tubal pregnancy was made before surgery; we were unable to obtain consent from the patient for bilateral salpingectomy as this would have resulted in loss of the ability to conceive naturally after the current pregnancy, and preservation of the fallopian tube was
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
2115
2116
30
35
31
29
38
39
28
32
34
32
Hanf 2
Dietz3
Jonler4
Wang5
Pan6
Hoopmann7
Bettocchi8
Nikolic9
Jeong10
This case
G1P0
G3P2
G2P1
G2P0
G0P0
G3P1
G0P0
G0P0
G2P2
G1P0
Parity
10
8
10
7
6
7
4
6
6
7
Gestational week
Clomiphene+AIH
Clomiphene
None
Gonadotrophin
ICSI
IVF-ET
GIFT
IVF-ET
Gonadotrophin
IVF-ET
Treatment for infertility
NA
NA
NA
NA
3
3
3
Unknown
NA
5
Number of ET
1
1
1
5
1
1
2
1
3
1
Intrauterine sac (n)
38 weeks cesarean section
Outcome
Laparoscopic bilateral salpingectomy D&C Laparoscopic salpingectomy+salpingotomy
Bilateral salpingectomy
Laparoscopic bilateral salpingostomy D&C Laparoscopic salpingectomy+salpingotomy
Bilateral salpingectomy
39 weeks normal vaginal delivery
Miscarriage
39 weeks normal vaginal delivery
Term twins after selective reduction
Miscarriage
Term normal vaginal delivery
Laparoscopic Miscarriage salpingectomy Salpingo-oophorectomy D&C Abortion Laparoscopic bilateral salpingotomy Expectant management 37 weeks twins cesarean section
Laparoscopic bilateral salpingectomy
Operation
AIH, artificial insemination with the husband’s semen; D&C, dilatation and curettage; ET, embryo transfer; GIFT, gamete intrafallopian transfer; ICSI, intracytoplasmic sperm injection; IVF, in vitro fertilization; NA, not applicable.
Age (years)
Author
Table 1 Case of bilateral tubal pregnancy and intrauterine pregnancies
T. Fukuda et al.
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
Heterotopic pregnancy
determined to be possible because the right tubal pregnancy site was small and had not ruptured. The possibility of persistent ectopic pregnancy might have remained after linear salpingotomy, and we thus carefully performed the procedure to leave no residual portion. In the previous case, a similar surgical procedure had also resulted in a full-term intrauterine pregnancy.8 In persistent ectopic pregnancy cases with hemoperitoneum, our intention is to repeat surgery. In vitro fertilization (IVF) has been improved to lower risks without compromising pregnancy rate. Cancellation of insemination or cryopreservation of excess embryos after IVF and increased use of elective singleembryo transfer can reduce multiple pregnancy.13 Frozen-thawed embryo transfer can reduce the incidence of ectopic pregnancy.14 It would thus seem that artificial insemination with the husband’s semen with ovarian stimulation is in effect the leading contributor to multiple births.15 In fact, recent reports indicate that the leading contributor is hyperovulation due to fertility drugs rather than IVF. In the past, there was a case in which a contralateral tubal pregnancy was detected during the postoperative period, leading to repeat surgery.3 When surgery is performed for patients diagnosed with ectopic pregnancy after the use of fertility drugs, surgeons need to thoroughly examine whether there is any other pregnancy site, including the contralateral fallopian tube. Above all, controlled ovarian stimulation is important to prevent multiple or heterotopic pregnancy.
Disclosure
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
None declared. 14.
References 1. Duce MN, Ozer C, Egilmez H, Apaydin FD, Yildiz A, Kara E. Heterotopic pregnancy: Case report. Abdo Imaging 2002; 27: 677–679. 2. Hanf V, Dietl J, Gagsteiger F, Pfeiffer KH. Bilateral tubal pregnancy with intra-uterine gestation after IVF-ET: Therapy
15.
by bilateral laparoscopic salpingectomy; a case report. Eur J Obstet Gynecol Reprod Biol 1990; 37: 87–90. Dietz TU, Haenggi W, Birkhaeuser M, Gyr T, Dreher E. Combined bilateral tubal and multiple intrauterine pregnancy after ovulation induction. Eur J Obstet Gynecol Reprod Biol 1993; 48: 69–71. Jonler M, Rasmussen KL, Lundoorff P. Coexistence of bilateral tubal and intrauterine pregnancy. Acta Obstet Gynecol Scand 1995; 74: 750–752. Wang YL, Yang TS, Chang SP, Ng HT. Heterotopic pregnancy after GIFT managed with expectancy: A case report. Chin Med J 1996; 58: 218–222. Pan HS, Chuang J, Chiu SF et al. Heterotopic triplet pregnancy: Report of a case with bilateral tubal pregnancy and an intrauterine pregnancy. Hum Reprod 2002; 17: 1363–1366. Hoopmann M, Wilhelm L, Possover M, Nawroth F. Heterotopic triplet pregnancy with bilateral tubal and intrauterine pregnancy after IVF. Reprod Biomed Online 2003; 6: 345–348. Bettocchi S, Nappi L, Ceci O et al. Simultaneous bilateral tubal pregnancies and intrauterine pregnancy with five fetuses. J Am Assoc Gynecol Laparosc 2004; 11: 195–196. Jeong HC, Park IH, Yoon YS et al. Heterotopic triplet pregnancy with bilateral tubal and intrauterine pregnancy after spontaneous conception. Eur J Obstet Gynecol Reprod Biol 2009; 142: 161–162. Nikolic B, Mitrovic A, Pavlovic DV, Cirovic DM, Dragojevic-Dikic S, Lukic R. Triple pregnancy: Intrauterine and bilateral tubal ectopic pregnancies. Aust N Z J Obstet Gynaecol 2004; 44: 260–261. Clayton HB, Schieve LA, Peterson HB, Jamieson DJ, Reynolds MA, Wright VC. A comparison of heterotopic and intrauterine-only pregnancy outcomes after assisted reproductive technologies in the United States from 1999 to 2002. Fertil Steril 2007; 71: 303–309. Takahashi A, Takahama J, Marugami N et al. Ectopic pregnancy: MRI findings and clinical utility. Abdom Imaging 2013; 38: 844–850. Stillman RJ, Richter KS, Banks NK, Graham JR. Elective single embryo transfer: A 6-year progressive implementation of 784 single blastocyst transfers and the influence of payment method on patient choice. Fertil Steril 2009; 92: 1895– 1906. Shapiro BS, Daneshmand ST, De Leon L, Garmer FC, Aguirre M, Hudson C. Frozen-thawed embryo transfer is associated with a significantly reduced incidence of ectopic pregnancy. Fertil Steril 2012; 98: 1490–1494. McClamrock HD, Jones HW Jr, Adashi EY. Ovarian stimulation and intrauterine insemination at the quarter centennial: Implications for the multiple births epidemic. Fertil Steril 2012; 97: 802–809.
© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology
2117
