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Diagnosis and Laparoscopic Management of 12 Consecutive Cases of Ovarian Pregnancy and Review of Literature
Clinical Opinion
Diagnosis and Laparoscopic Management of 12 Consecutive Cases of Ovarian Pregnancy and Review of Literature F. Odejinmi, M. I. Rizzuto,* R. MacRae, O. Olowu, and M. Hussain From the Department of Obstetrics and Gynaecology, Whipps Cross University Hospital, London, UK.
ABSTRACT We sought to determine the outcome of the laparoscopic management of ovarian ectopic pregnancy (OEP) in a United Kingdom district general hospital and reviewed the literature. We conducted a 5-year prospective cohort study of the management of OEP cases between January 2003 and January 2008. Twelve patients had OEP confirmed with histology among a cohort of 421 ectopic pregnancies. The mean gestational age was 45 days. All 12 patients had abdominal pain and 4 (33%) had vaginal bleeding. One (8%) patient became hypovolemic before laparoscopy. Four (33%) women had risk factors for ectopic pregnancy, 2 of whom were current intra-uterine contraceptive users. Preoperative diagnosis of ectopic pregnancy was made in 11 (92%) of 12 patients by transvaginal ultrasonography and OEP in 9 (75%) patients. All cases were managed by laparoscopic surgery with no conversion to laparotomy. The ovarian pregnancy was resected and the ovary conserved in 11 (92%) patients with only 1 requiring an oophorectomy. The mean operating time was 49 minutes. None of the patients needed further treatment. No complications occurred after laparoscopic surgery and the mean hospital stay was 2 days. Considering the rarity of ovarian pregnancy, this is one of the largest series of patients with OEP treated exclusively by laparoscopic surgery and highlights our recent experience of performing conservative laparoscopic surgery for most of our patients. Journal of Minimally Invasive Gynecology (2009) 16, 354–9 Ó 2009 AAGL. All rights reserved. Keywords:
Ovarian ectopic; Laparoscopy; Wedge resection
Primary ovarian ectopic pregnancy (OEP), the implantation of the gestational sac in the ovary, is one of the rarest forms of ectopic pregnancy. Its incidence after natural conception ranges from 1 in 2000 to 1 in 60 000 deliveries and accounts for the 3% of all ectopic pregnancies [1,2]. Since the first case, reported by Saint Maurice of France in 1682 [3], the incidence is thought to be increasing because of improved diagnostic techniques and assisted reproductive technology [4]. Diagnosis and treatment of this condition continues to challenge practicing clinicians because no typical risk factors exist compared with other types of ectopic pregnancy, and when signs and symptoms occur they are similar to those encountered in tubal pregnancies and ruptured corpus luteal cysts. Endoscopic surgery is now regarded as the criterion standard for the surgical management of ectopic pregnancy (Royal College of Obstetricians and Gynecologists), howThe authors have no commercial, proprietary, or financial interest in the products or companies described in this article. Corresponding author: M. Ivana Rizzuto. E-mail: [email protected] Submitted November 20, 2008. Accepted for publication January 8, 2009. Available at www.sciencedirect.com and www.jmig.org 1553-4650/$ - see front matter Ó 2009 AAGL. All rights reserved. doi:10.1016/j.jmig.2009.01.002
ever, in only a few case series was operative laparoscopy used exclusively for the treatment of women with OEP [1,5], and in most case reports open surgery is still used for the treatment of women with ovarian pregnancy despite the benefits of the minimal access approach. In this article we describe our experience with 12 consecutive cases of OEP, which were diagnosed and successfully treated by laparoscopy in our hospital during a period of 5 years and we review the literature on endoscopic surgery for the management of ovarian gestation.
Methods We conducted a MEDLINE search of the English-language literature using the terms ‘‘ovarian pregnancy/ovarian ectopic pregnancy’’ and ‘‘laparoscopy/laparoscopic surgery’’ of articles published from 1950 through 2008. We then hand searched the references of identified relevant articles and included them in our review. The first mention of laparoscopic surgery for the management of ovarian ectopic pregnancy was in 1988 [6]. The largest case series where laparoscopy was used exclusively to treat women with ovarian pregnancy was published in 1997
Odejinmi et al.
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355 Table 1
[1]. We compared the operative laparoscopy rates in case reports from 1988 through 1997 with those from 1998 through 2008. We also compared the operative laparoscopy rates reported from case series of more than 2 patients that reported the use of operative laparoscopy for the treatment of women with ovarian pregnancy with our case series of 12 patients. Between January 2003 and January 2008 information was collected prospectively from all women diagnosed with OEP at our university hospital and kept in a computer database (Access, Microsoft Inc., Redmond, WA), and these data were used for comparison. Results are expressed as proportions, means, and SD of the means. In our series, information was collected on patient age, symptoms, duration of amenorrhea, intra-uterine contraceptive device use, preoperative diagnosis by ultrasound, intraoperative diagnosis, and postoperative outcome. The diagnosis of ovarian pregnancy was established by review of the pathological reports from surgical material in all ectopic pregnancies and the histopathologic examination was based on the 4 criteria of Otto Spiegelberg [7] (Table 1). Ovarian wedge resection was carried out using monopolar electrodissection with the electrosurgical generator set at 50W. The ovary was continuously irrigated during the procedure and hemostasis achieved using bipolar diathermy set at 35 W. The ovaries were not oversewn.
Spielberg’s criteria [7] 1. 2. 3. 4.
The tube and fimbria on the affected side must be intact and clearly separate from the ovary The gestation sac must occupy the position of the ovary The ovary must be connected to the uterus by the ovarian ligament Definite ovarian tissue must be found in the sac wall (chorionic villi in the ovary and not fallopian tube)
At ultrasound scan a diagnosis of ectopic pregnancy was made in 92% (11/12) of cases and of OEP in 75% (9/12). All our patients had serum b-human chorionic gonadotropin (hCG) estimations above 1000 IU/mL. An OEP was diagnosed in 92% of cases at laparoscopy. In 1 case an initial misdiagnosis of ruptured corpus luteum occurred, which was later diagnosed histologically as an ovarian pregnancy. All cases were managed by laparoscopic surgery and no conversion to laparotomy occurred. The ovary was conserved by performing a wedge resection in 92% (11/12) of cases. The mean total blood loss was 730 mL with 1 patient in circulatory collapse with a blood loss of 3000 mL. The mean operating time was 49 6 10 minutes and mean hospital stay was 1.6 6 1 day. No complications occurred after laparoscopic surgery and none of the patients needed further treatment. Literature Search The results of the literature search are outlined in Fig. 1. Between 1950 and 2008 we identified 443 publications referring to OEP with 258 published in the English language. During this period 191 case reports and 42 case series discussed surgical management of OEP. From 1988 (when the first laparoscopic surgery for OEP was reported) through 2008 we identified 94 case reports and 17 case series on the surgical management of OEP. Between 1973 and 1996, laparoscopic surgery for OEP was reported in 26% of case reports. After the first reported series managed exclusively by laparoscopic surgery in 1997, laparoscopic surgery was performed in 51% of case
Results Case Series Twelve cases of ovarian pregnancy were diagnosed in our department between January 2003 and January 2008. This represented 2.9% (12/421) of ectopic pregnancies and 1 case for every 2070 deliveries during the study period. Information about the patients, their diagnosis, and their treatment is illustrated in Table 2. The mean age, parity, and gestational age was 31 6 7.2 years, 1.4, and 6 6 1.5 weeks, respectively. Two (16.6%) patients had history of IUCD use. Table 2
Cases of ovarian ectopic pregnancy Case No.
Age (yrs)
Parity
IUCD use
GA
Scan preoperative diagnosis
Intraoperative diagnosis
Side
Hemoperitoneum
Procedure
LOS (days)
Operative time (min)
1 2 3 4 5 6 7 8 9 10 11 12
30 19 42 34 22 33 22 26 35 37 33 38
0 0 4 0 0 3 0 1 1 4 1 3
Y N N N N N N N N N N Y
5 6 9 6 7 4 8 5 7 5 4 6
OEP OEP OEP OEP OEP OEP EP OEP OEP OEP Ruptured CL EP
OEP OEP OEP OEP OEP OEP OEP OEP OEP OEP CL OEP
LT LT LT RT RT RT RT RT LT LT LT LT
500 300 200 300 1500 400 100 700 3000 300 1400 100
WR WR O WR WR WR WR WR WR WR WR WR
1 2 3 1 1 4 1 1 2 1 1 1
30 60 40 45 60 40 60 50 60 45 NR 50
CL 5 Corpus luteum; EP 5 ectopic pregnancy; GA 5 gestational age; LOS 5 length of stay; LT 5 left; N 5 no; O 5 oophorectomy; OEP 5 ovarian ectopic pregnancy; RT 5 right; WR 5 wedge resection; Y 5 yes; IUCD5 intra-uterine contraceptive device; NR5 not reported.
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Fig. 1. Cases of ovarian ectopic pregnancy.
reports published from 1997 through 2008. This represented a statistically significant increase (c2 5 4.9, p 5.02) in the use of laparoscopic surgery for the management of OEP. Where the type of surgery used was mentioned in the article (wedge resection or partial oophorectomy) ovarian conservation was performed in 27 (84%) of 32 in the laparoscopy group compared with 33 (70%) of 46 in the laparotomy group. Although a greater number of women who had operative laparoscopy had more conservative surgery (resection of the ectopic with conservation of ovarian tissue; 84% vs 70%), the difference is not statistically significant (p 5.715). We identified 4 case series published from 1988 through 2008 reporting more than 2 cases of OEP managed by operative laparoscopy. The patient characteristics, diagnosis, and management from these series are compared with those from our study in Tables 3 and 4. These indicate that although patient characteristics are similar, an improving trend exists in the diagnosis and laparoscopic management of OEP.
on the population studied. In our hospital during the study period ovarian pregnancy represented 2.9% (12/421) of all ectopic pregnancies, which meant 1 case for every 2070 deliveries. Traditional risk factors for tubal ectopic pregnancy were not relevant risk factors for ovarian pregnancies [1,12,14]. Reports exist of ovarian pregnancy associated with ovulation stimulation and assisted conception techniques [15–17]. However, based on a large series of 1800 ectopic pregnancies during a 10-year study the only risk factor associated with the site of ectopic pregnancy was current use of an intrauterine device (IUD). This was associated with distal ectopic pregnancies and ovarian pregnancies [18]. This phenomenon was explained on the basis that although the IUCD reduces intrauterine implantation it does not have the same protective effect against ovarian pregnancies [19]. However, different studies report wide variations in the proportion of patients with ovarian pregnancy using the IUCD. These range from 16% in our study to 70% in another study [14] (Table 3). This wide variation may partly be explained on the different prevalence of IUCD use in the general population. The absence of a strong association between the IUCD and ovarian pregnancy in our study would suggest that yet unidentified factors are at play. Patients with OEP usually have the same symptoms as those with tubal ectopic pregnancy [1,20]. As in our study, the typical symptoms are abdominal pain and vaginal
Discussion Primary OEP is a rare variant of ectopic pregnancy and its incidence is estimated at 1% to 3% of diagnosed ectopic pregnancies [2,8,9]. The true incidence is believed by some authors to be higher as some women treated medically for pregnancy of unknown location may have ovarian pregnancies [10,11]. The incidence is also believed to vary depending Table 3
Comparison of patient demographics Authors
Publication year
Duration of study
Years of study
No. of patients
Wks of amenorrhea, mean (range)
Age (yrs), mean 6 SD
Mean parity (yrs)
IUCD use
Vasilev and Sauer [13] Morice et al [5] Sienera et al [1] Raziel et al [8] Current study
1990 1996 1997 2004 2009
4 10 12 12 5
1982–1986 1983–1993 1984–1995 1990–2001 2003–2008
10 4 8 19 12
6 (3–10) 7.25 (6–9) 6.7 (5–11) N/R 6 (4–9)
26.5 6 3.7 33 6 4 32 6 3.3 32 6 5.7 30 6 7
3.6 N/R N/R 2 1.4
70% 25% 38% 70% 16%
IUCD 5 intra-uterine contraceptive device; N/R 5 not rated.
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Table 4
Diagnosis and management comparison Authors Vasilev and Sauer [13] Morice et al [5] Seinera et al [1] Raziel et al [11] Current study
Preoperative diagnosis OEP
Preoperative diagnosis ectopic
N/R
40% (OEP only)
25%
100% 75% 95% 92%
5% 75%
Operative laparoscopy
Laparotomy
Medical
Oophorectomy
Resection
10%
90%
0%
20%
80%
100% 100% 50% 100%
0% 0 40% 0%
0% 0% 10% 0%
0% 0 20% 8%
100% 100% 70% 92%
Hemoperitoneum, mean (range)
Operative time (min)
368 (0–900) 300 (100–700) 125 (N/R) N/R 733 (100–3000)
N/R 25–45 30–60
OEP 5 Ovarian ectopic pregnancy; N/R 5 not reported.
bleeding. Circulatory collapse was present in 1 (8%) of 12 patients in our study. However, the reported incidence of circulatory collapse varies with different studies. In 2004, the incidence of circulatory collapse was reported as 23% between 1971 and 1989 and 30% between 1990 and 2000 [21]. In a series of 8 cases, none of the patients had circulatory collapse [1]. These differences may be a reflection of how early diagnosis is made. The mean duration from the last menstrual period to diagnosis is reported to be 6 to 7.25 weeks by some of the large case series (Table 3). However, reports in the literature also exist of late diagnosis and ovarian pregnancies surviving to advanced gestation. Seki et al (1997) [22] described an ovarian pregnancy diagnosed at cesarean section performed at 30 weeks’ gestation and a different study [23] described a case of full-term ovarian pregnancy. In 1998, a case of heterotopic ovarian pregnancy proceeding to term was reported [24]. The diagnosis of ovarian pregnancy remains a challenge and many cases are still missed at ultrasonography [25]. The criteria for diagnosing ovarian pregnancy are mainly surgical and cannot be established by ultrasonography [27]. In spite of this limitation, increasingly more cases are diagnosed at ultrasonography. In 1990 authors reported 40% of their cases diagnosed preoperatively as ectopic pregnancies on ultrasonography [14]. Years later, other authors reported 75% to 100% of their cases diagnosed as ectopic gestation on ultrasonography (Table 4). However, until recently a definitive diagnosis of OEP on ultrasound scan was made in only a few cases (Table 4). The view was expressed that the difficulty in making a definitive diagnosis of OEP on ultrasonography limits the use of medical treatment as laparoscopy is usually needed for diagnosis. Our study suggests an improvement in the definitive diagnosis of ovarian pregnancy. This could be attributed to the reporting of sonographic features of OEP and increasing ultrasonography experience. A number of authors have described the presence of a ringlike echogenic structure on the surface or in the substance of the ovary [26–30]. Ultrasonographic images of ovarian ectopics were published with wide echogenic rings and small internal echolucent areas [31]. The echogenic ring was absent in the only patient with a ruptured OEP. The echogenicity of the ring was greater than the ovary in the other 5 cases. This is an important sonographic feature as a corpus luteum in
pregnancy may also have a ringlike appearance on ultrasonography. Various authors have reported the corpus luteum to be of less or equal echogenicity to the ovary in most cases whereas ectopics (tubal or ovarian) were usually more echogenic than the ovary or corpus luteum [32–34]. In our experience the ovarian ectopic was more echogenic than the surrounding ovarian tissue (Fig. 2) in keeping with the findings of these authors. The presence of a yolk sac or fetal pole in the ovary makes the diagnosis easier but these are reported to be less common findings [32]. A fetal pole was identified in only 1 (8%) of our cases. We share the view of other authors [12] that serum b-hCG measurements are a useful diagnostic tool when ultrasound scan findings are inconclusive. Ovarian ectopics were associated with low (,1000 IU/L) serum b-hCG levels [25]. This was not our experience as most of our patients had serum b-hCG levels greater than 1000 IU/L. Typically the ovarian ectopic has the appearance of a hemorrhagic ovarian mass (Fig. 3) at surgery. However, ovarian ectopics can also pose a diagnostic dilemma at surgery as they can be misdiagnosed as hemorrhagic corpus luteum or ovarian cysts. [25,26]. This is illustrated by one of our cases initially thought to be a ruptured corpus luteum and later confirmed to be an ovarian ectopic at histology. In an attempt at resolving this diagnostic dilemma, a study advised that an ovarian hemorrhagic mass associated with normal tubes, a serum concentration of hCG greater than 1000 IU/mL, and
Fig. 2. Ultrasound image of ovarian pregnancy.
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In view of concerns about future fertility, current practice is to resect the ovarian pregnancy and preserve healthy ovarian tissue. Oophorectomy is rarely indicated. Our ovarian pregnancy resection rate of 92% by laparoscopy is one of the highest in the published literature (Table 4). Trophoblastic tissue may persist after resection of the pregnancy making further treatment necessary. For this reason, follow-up hCG levels must be obtained. However, none of our patients required further treatment. It is also noteworthy that operating time was short (mean 49 minutes) and no complications occurred. Our experience with laparoscopic management of OEP reveals that it is effective, safe, and conserves ovarian function in most cases. In addition, it offers a short hospital stay, requires minimal follow-up, and allows the patient to resume normal activity within a short period of time. Fig. 3. Laparoscopic image of ovarian pregnancy.
absent intrauterine sac suggests an ovarian pregnancy [1]. This serves as a useful guide, with the main limitation being cases with hCG less than 1000 IU/L. A review of the literature on the management of ovarian pregnancy reveals that surgery is currently the mainstay of management and medical management is still less frequently performed (Table 4). The first reported case of successful medical management of OEP with methotrexate was in 1988 [34]. Subsequently, other successful cases were reported [35,36]. Medical management has the advantage of being less invasive than surgery. However, its use appears to be limited by the need to perform diagnostic laparoscopy in many cases. Many authors share the view that if laparoscopy is required for diagnosis, definitive surgical management should be performed at the same time [34]. However, cases of medical treatment performed after laparoscopy are reported [35]. We anticipate that the positive trend in the definitive diagnosis of ovarian pregnancy by ultrasonography will in future increase the proportion of cases managed medically. Increasingly, operative laparoscopy is the method of choice in the surgical management of OEP [14] since the first reported case in 1988 [6]. A review of case reports on the surgical management of ovarian ectopics reveals that operative laparoscopy was performed in 26% of cases from 1988 through 1997 and in 51% of cases from 1998 through 2008 (Fig. 1). Likewise, a review of case series indicates an increase in operative laparoscopy rate from 10% [14] to 100% in our study (Table 4). Significant hemoperitoneum was reported as a common indication to convert from laparoscopy to laparotomy [14]. However, in our experience this is no longer an absolute indication for conversion to laparotomy as illustrated in one of our cases when operative laparoscopy was performed in the presence of significant hemoperitoneum of 3000 mL (Table 2) and in other reports in literature [37], but laparoscopy under these circumstances depends on surgical expertise and adequate resuscitation of the patient.
References 1. Seinera P, Di Gregorio A, Arisio R, Decko A, Crana F. Ovarian pregnancy and operative laparoscopy: report of eight cases. Hum Reprod. 1997;12:608–610. 2. Grimes HG, Nosal RA, Gallagher JC. Ovarian pregnancy: a series of 24 cases. Obstet Gynecol. 1983;61:174–180. 3. Lurie S. The history of the diagnosis and treatment of ectopic pregnancy: a medical adventure. Eur J Obstet Gynecol Reprod Biol. 1992;43:1–7. 4. Abidi A, Gordon R, Harman MB, Pinto M. Ovarian pregnancy without definitive pathologic confirmation: a case report. J Reprod Med. 2007; 52:320–322. 5. Morice P, Dubuisson JB, Chapron C, De Gaffier A, Mouelhi T. Laparoscopic management of ovarian pregnancy. Gynecol Endosc. 1996;5: 247–249. 6. Van Coevering RJ, Fisher JE. Laparoscopic management of ovarian pregnancy: a case report. J Reprod Med. 1988;33:774–776. 7. Spiegelberg O. Zur Cosuistik der Ovarialschwanger schalt. Arch Gynaekol. 1973;13:73–76. 8. Gaudoin MR, Coulter KL, Robins AM, Verghese A, Hanretty KP. Is the incidence of ovarian ectopic pregnancy increasing? Eur J Obstet Gynecol Reprod Biol. 1996;70:141–143. 9. Raziel A, Schachter M, Mordechai E, Friedler S, Pansky M, Ron-El R. Ovarian pregnancy: a 12-year experience of 19 cases in one institution. Eur J Obstet Gynecol Reprod Med. 2004;114:92–96. 10. Sijanovic S, Topolovec Z, Sijanovic I. Laparoscopic treatment of primary ovarian pregnancy. J Am Assoc Gynecol Laparosc. 2002;9: 221–222. 11. Raziel A, Golan A, Pansky M, Ron-El R, Bukovsky I, Caspi E. Ovarian pregnancy: a report of twenty cases in one institution. Am J Obstet Gynecol. 1990;163:1182–1185. 12. Stovall TG, McCord ML. Early pregnancy loss and ectopic pregnancy. In: Berek S, Adush: EY, ed. Novak’s Gynecology. 12th ed. Baltimore: Williams and Wilkins; 1996. p. 491. 13. Hallatt J. Primary ovarian pregnancy: a report of twenty-five cases. Am J Obstet Gynecol. 2005;143:55–60. 14. Vasilev S, Sauer M. Diagnosis and modern surgical management of ovarian pregnancy. Gynecol Obstet. 1990;170:395–398. 15. Selo-Ojeme DO, GoodFellow CF. Simultaneous intrauterine and ovarian pregnancy following treatment with clomiphene citrate. Arch Gynecol Obstet. 2002;266:232–234. 16. Bontis J, Grimbizis G, Tarlatzis BC, Miliaras D, Bili H. Intrafollicular ovarian pregnancy after ovulation/intrauterine insemination: pathophysiological aspects and diagnostic problems. Hum Reprod. 1997;12: 376–378. 17. Shibahara H, Funabiki M, Shiotani T, Ikeda Y, Koyama K. A case of primary ovarian pregnancy after in vitro fertilization and embryo transfer. J Assist Reprod Genet. 1997;14:63–64.
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18. Bouyer J, Coste J, Fernandez H, et al. Sites of ectopic pregnancy: a 10year population-based study of 1800 cases. Hum Reprod. 2002;17: 3224–3230. 19. Lehfeldt H, Tietze C, Gorstein F. Ovarian pregnancy and the intrauterine device. Am J Obstet Gynecol. 1970;108:1105–1109. 20. Cheng CC, Seow KM, Huang LW, Chen HH, Hwang JL. Laparoscopic management of primary ovarian pregnancy. J Gynecol Surg. 2000;16: 155–159. 21. Raziel A, Mordechai E, Schachter M, Friedler S, Pansky M, Ron-El R. A comparison of the incidence, presentation, and management of ovarian pregnancies between two periods of time. J Am Assoc Gynecol Laparosc. 2004;11:191–194. 22. Seki H, Kuromaki K, Takeda S, Kinoshita K. Ovarian pregnancy diagnosed in the third trimester: a case report. J Obstet Gynaecol Res. 1997; 24:109–114. 23. Sehgal A, Goyal LD, Goel P, Sunita BS. Full term ovarian pregnancy: a case report. Aust N Z J Obstet Gynaecol. 2005;45:165–166. 24. Shahabuddin AK, Chowdhury S. Primary term ovarian pregnancy superimposed by intrauterine pregnancy: a case report. J Obstet Gynaecol Res. 1998;24:109–114. 25. Oliver R, Malik M, Coker A, Morris J. Management of extra-tubal and rare ectopic pregnancies: case series and review of current literature. Arch Gynecol Obstet. 2007;276:125–131. 26. Marcus SF, Brinsden PR. Primary ovarian pregnancy after in vitro fertilization and embryo transfer: report of seven cases. Fertil Steril. 1993;60:167–169.
359 27. Honigl W, Reich O. Vaginal ultrasound in ovarian pregnancy. Ultraschall Med. 1997;18:233–236. 28. Aztori E. Transvaginal ultrasonography in the ovarian pregnancy: case report. Ultrasound Obstet Gynecol. 1993;3:217–218. 29. Varras M, Polizos D, Kalamra C, et al. Primary ruptured ovarian pregnancy in a spontaneous conception cycle: a case report and review of the literature. Clin Exp Obstet Gynecol. 2002;29:143–147. 30. Athey PA, Jayson HT, Rolando E, Watson AB. Sonographic findings in primary ovarian pregnancy. J Clin Ultrasound. 1990;18:730–732. 31. Comstock C, Huston K, Lee W. The ultrasonographic appearance of ovarian ectopic pregnancies. Obstet Gynecol. 2005;105:42–45. 32. Frates MC, Visweswaran A, Laing FC. Comparison of tubal ring and corpus luteum echogenicities: a differentiating characteristic. J Ultrasound Med. 2001;20:27–31. 33. Stein MW, Ricci ZJ, Novak L, Robert SJH, Koenigsberg M. Sonographic comparison of the tubal ring of ectopic pregnancy with the corpus luteum. J Ultrasound Med. 2004;23:57–62. 34. Kudo M, Tanaka T, Fujinka S. A successful treatment of left ovarian pregnancy with methotrexate. Nippon Sanka Fujinka Zasshi. 1988;40: 811–813. 35. Mittal S, Dadhwal V, Baurasi P. Successful medical management of ovarian pregnancy. Gynecol Obstet. 2003;80:309–310. 36. Kiran G, Guvan AM, Kostu B. Systemic medical management of ovarian pregnancy. Int J Gynecol Obstet. 2005;91:177–178. 37. Rizzuto MI, Oliver R, Odejinmi F. Laparoscopic management of ectopic pregnancy in the presence of a significant hemoperitoneum. Arch Gynecol Obstet. 2008;277:433–436.
Diagnosis and Laparoscopic Management of 12 Consecutive Cases of Ovarian Pregnancy and Review of Literature F. Odejinmi, M. I. Rizzuto,* R. MacRae, O. Olowu, and M. Hussain From the Department of Obstetrics and Gynaecology, Whipps Cross University Hospital, London, UK.
ABSTRACT We sought to determine the outcome of the laparoscopic management of ovarian ectopic pregnancy (OEP) in a United Kingdom district general hospital and reviewed the literature. We conducted a 5-year prospective cohort study of the management of OEP cases between January 2003 and January 2008. Twelve patients had OEP confirmed with histology among a cohort of 421 ectopic pregnancies. The mean gestational age was 45 days. All 12 patients had abdominal pain and 4 (33%) had vaginal bleeding. One (8%) patient became hypovolemic before laparoscopy. Four (33%) women had risk factors for ectopic pregnancy, 2 of whom were current intra-uterine contraceptive users. Preoperative diagnosis of ectopic pregnancy was made in 11 (92%) of 12 patients by transvaginal ultrasonography and OEP in 9 (75%) patients. All cases were managed by laparoscopic surgery with no conversion to laparotomy. The ovarian pregnancy was resected and the ovary conserved in 11 (92%) patients with only 1 requiring an oophorectomy. The mean operating time was 49 minutes. None of the patients needed further treatment. No complications occurred after laparoscopic surgery and the mean hospital stay was 2 days. Considering the rarity of ovarian pregnancy, this is one of the largest series of patients with OEP treated exclusively by laparoscopic surgery and highlights our recent experience of performing conservative laparoscopic surgery for most of our patients. Journal of Minimally Invasive Gynecology (2009) 16, 354–9 Ó 2009 AAGL. All rights reserved. Keywords:
Ovarian ectopic; Laparoscopy; Wedge resection
Primary ovarian ectopic pregnancy (OEP), the implantation of the gestational sac in the ovary, is one of the rarest forms of ectopic pregnancy. Its incidence after natural conception ranges from 1 in 2000 to 1 in 60 000 deliveries and accounts for the 3% of all ectopic pregnancies [1,2]. Since the first case, reported by Saint Maurice of France in 1682 [3], the incidence is thought to be increasing because of improved diagnostic techniques and assisted reproductive technology [4]. Diagnosis and treatment of this condition continues to challenge practicing clinicians because no typical risk factors exist compared with other types of ectopic pregnancy, and when signs and symptoms occur they are similar to those encountered in tubal pregnancies and ruptured corpus luteal cysts. Endoscopic surgery is now regarded as the criterion standard for the surgical management of ectopic pregnancy (Royal College of Obstetricians and Gynecologists), howThe authors have no commercial, proprietary, or financial interest in the products or companies described in this article. Corresponding author: M. Ivana Rizzuto. E-mail: [email protected] Submitted November 20, 2008. Accepted for publication January 8, 2009. Available at www.sciencedirect.com and www.jmig.org 1553-4650/$ - see front matter Ó 2009 AAGL. All rights reserved. doi:10.1016/j.jmig.2009.01.002
ever, in only a few case series was operative laparoscopy used exclusively for the treatment of women with OEP [1,5], and in most case reports open surgery is still used for the treatment of women with ovarian pregnancy despite the benefits of the minimal access approach. In this article we describe our experience with 12 consecutive cases of OEP, which were diagnosed and successfully treated by laparoscopy in our hospital during a period of 5 years and we review the literature on endoscopic surgery for the management of ovarian gestation.
Methods We conducted a MEDLINE search of the English-language literature using the terms ‘‘ovarian pregnancy/ovarian ectopic pregnancy’’ and ‘‘laparoscopy/laparoscopic surgery’’ of articles published from 1950 through 2008. We then hand searched the references of identified relevant articles and included them in our review. The first mention of laparoscopic surgery for the management of ovarian ectopic pregnancy was in 1988 [6]. The largest case series where laparoscopy was used exclusively to treat women with ovarian pregnancy was published in 1997
Odejinmi et al.
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355 Table 1
[1]. We compared the operative laparoscopy rates in case reports from 1988 through 1997 with those from 1998 through 2008. We also compared the operative laparoscopy rates reported from case series of more than 2 patients that reported the use of operative laparoscopy for the treatment of women with ovarian pregnancy with our case series of 12 patients. Between January 2003 and January 2008 information was collected prospectively from all women diagnosed with OEP at our university hospital and kept in a computer database (Access, Microsoft Inc., Redmond, WA), and these data were used for comparison. Results are expressed as proportions, means, and SD of the means. In our series, information was collected on patient age, symptoms, duration of amenorrhea, intra-uterine contraceptive device use, preoperative diagnosis by ultrasound, intraoperative diagnosis, and postoperative outcome. The diagnosis of ovarian pregnancy was established by review of the pathological reports from surgical material in all ectopic pregnancies and the histopathologic examination was based on the 4 criteria of Otto Spiegelberg [7] (Table 1). Ovarian wedge resection was carried out using monopolar electrodissection with the electrosurgical generator set at 50W. The ovary was continuously irrigated during the procedure and hemostasis achieved using bipolar diathermy set at 35 W. The ovaries were not oversewn.
Spielberg’s criteria [7] 1. 2. 3. 4.
The tube and fimbria on the affected side must be intact and clearly separate from the ovary The gestation sac must occupy the position of the ovary The ovary must be connected to the uterus by the ovarian ligament Definite ovarian tissue must be found in the sac wall (chorionic villi in the ovary and not fallopian tube)
At ultrasound scan a diagnosis of ectopic pregnancy was made in 92% (11/12) of cases and of OEP in 75% (9/12). All our patients had serum b-human chorionic gonadotropin (hCG) estimations above 1000 IU/mL. An OEP was diagnosed in 92% of cases at laparoscopy. In 1 case an initial misdiagnosis of ruptured corpus luteum occurred, which was later diagnosed histologically as an ovarian pregnancy. All cases were managed by laparoscopic surgery and no conversion to laparotomy occurred. The ovary was conserved by performing a wedge resection in 92% (11/12) of cases. The mean total blood loss was 730 mL with 1 patient in circulatory collapse with a blood loss of 3000 mL. The mean operating time was 49 6 10 minutes and mean hospital stay was 1.6 6 1 day. No complications occurred after laparoscopic surgery and none of the patients needed further treatment. Literature Search The results of the literature search are outlined in Fig. 1. Between 1950 and 2008 we identified 443 publications referring to OEP with 258 published in the English language. During this period 191 case reports and 42 case series discussed surgical management of OEP. From 1988 (when the first laparoscopic surgery for OEP was reported) through 2008 we identified 94 case reports and 17 case series on the surgical management of OEP. Between 1973 and 1996, laparoscopic surgery for OEP was reported in 26% of case reports. After the first reported series managed exclusively by laparoscopic surgery in 1997, laparoscopic surgery was performed in 51% of case
Results Case Series Twelve cases of ovarian pregnancy were diagnosed in our department between January 2003 and January 2008. This represented 2.9% (12/421) of ectopic pregnancies and 1 case for every 2070 deliveries during the study period. Information about the patients, their diagnosis, and their treatment is illustrated in Table 2. The mean age, parity, and gestational age was 31 6 7.2 years, 1.4, and 6 6 1.5 weeks, respectively. Two (16.6%) patients had history of IUCD use. Table 2
Cases of ovarian ectopic pregnancy Case No.
Age (yrs)
Parity
IUCD use
GA
Scan preoperative diagnosis
Intraoperative diagnosis
Side
Hemoperitoneum
Procedure
LOS (days)
Operative time (min)
1 2 3 4 5 6 7 8 9 10 11 12
30 19 42 34 22 33 22 26 35 37 33 38
0 0 4 0 0 3 0 1 1 4 1 3
Y N N N N N N N N N N Y
5 6 9 6 7 4 8 5 7 5 4 6
OEP OEP OEP OEP OEP OEP EP OEP OEP OEP Ruptured CL EP
OEP OEP OEP OEP OEP OEP OEP OEP OEP OEP CL OEP
LT LT LT RT RT RT RT RT LT LT LT LT
500 300 200 300 1500 400 100 700 3000 300 1400 100
WR WR O WR WR WR WR WR WR WR WR WR
1 2 3 1 1 4 1 1 2 1 1 1
30 60 40 45 60 40 60 50 60 45 NR 50
CL 5 Corpus luteum; EP 5 ectopic pregnancy; GA 5 gestational age; LOS 5 length of stay; LT 5 left; N 5 no; O 5 oophorectomy; OEP 5 ovarian ectopic pregnancy; RT 5 right; WR 5 wedge resection; Y 5 yes; IUCD5 intra-uterine contraceptive device; NR5 not reported.
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Fig. 1. Cases of ovarian ectopic pregnancy.
reports published from 1997 through 2008. This represented a statistically significant increase (c2 5 4.9, p 5.02) in the use of laparoscopic surgery for the management of OEP. Where the type of surgery used was mentioned in the article (wedge resection or partial oophorectomy) ovarian conservation was performed in 27 (84%) of 32 in the laparoscopy group compared with 33 (70%) of 46 in the laparotomy group. Although a greater number of women who had operative laparoscopy had more conservative surgery (resection of the ectopic with conservation of ovarian tissue; 84% vs 70%), the difference is not statistically significant (p 5.715). We identified 4 case series published from 1988 through 2008 reporting more than 2 cases of OEP managed by operative laparoscopy. The patient characteristics, diagnosis, and management from these series are compared with those from our study in Tables 3 and 4. These indicate that although patient characteristics are similar, an improving trend exists in the diagnosis and laparoscopic management of OEP.
on the population studied. In our hospital during the study period ovarian pregnancy represented 2.9% (12/421) of all ectopic pregnancies, which meant 1 case for every 2070 deliveries. Traditional risk factors for tubal ectopic pregnancy were not relevant risk factors for ovarian pregnancies [1,12,14]. Reports exist of ovarian pregnancy associated with ovulation stimulation and assisted conception techniques [15–17]. However, based on a large series of 1800 ectopic pregnancies during a 10-year study the only risk factor associated with the site of ectopic pregnancy was current use of an intrauterine device (IUD). This was associated with distal ectopic pregnancies and ovarian pregnancies [18]. This phenomenon was explained on the basis that although the IUCD reduces intrauterine implantation it does not have the same protective effect against ovarian pregnancies [19]. However, different studies report wide variations in the proportion of patients with ovarian pregnancy using the IUCD. These range from 16% in our study to 70% in another study [14] (Table 3). This wide variation may partly be explained on the different prevalence of IUCD use in the general population. The absence of a strong association between the IUCD and ovarian pregnancy in our study would suggest that yet unidentified factors are at play. Patients with OEP usually have the same symptoms as those with tubal ectopic pregnancy [1,20]. As in our study, the typical symptoms are abdominal pain and vaginal
Discussion Primary OEP is a rare variant of ectopic pregnancy and its incidence is estimated at 1% to 3% of diagnosed ectopic pregnancies [2,8,9]. The true incidence is believed by some authors to be higher as some women treated medically for pregnancy of unknown location may have ovarian pregnancies [10,11]. The incidence is also believed to vary depending Table 3
Comparison of patient demographics Authors
Publication year
Duration of study
Years of study
No. of patients
Wks of amenorrhea, mean (range)
Age (yrs), mean 6 SD
Mean parity (yrs)
IUCD use
Vasilev and Sauer [13] Morice et al [5] Sienera et al [1] Raziel et al [8] Current study
1990 1996 1997 2004 2009
4 10 12 12 5
1982–1986 1983–1993 1984–1995 1990–2001 2003–2008
10 4 8 19 12
6 (3–10) 7.25 (6–9) 6.7 (5–11) N/R 6 (4–9)
26.5 6 3.7 33 6 4 32 6 3.3 32 6 5.7 30 6 7
3.6 N/R N/R 2 1.4
70% 25% 38% 70% 16%
IUCD 5 intra-uterine contraceptive device; N/R 5 not rated.
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Table 4
Diagnosis and management comparison Authors Vasilev and Sauer [13] Morice et al [5] Seinera et al [1] Raziel et al [11] Current study
Preoperative diagnosis OEP
Preoperative diagnosis ectopic
N/R
40% (OEP only)
25%
100% 75% 95% 92%
5% 75%
Operative laparoscopy
Laparotomy
Medical
Oophorectomy
Resection
10%
90%
0%
20%
80%
100% 100% 50% 100%
0% 0 40% 0%
0% 0% 10% 0%
0% 0 20% 8%
100% 100% 70% 92%
Hemoperitoneum, mean (range)
Operative time (min)
368 (0–900) 300 (100–700) 125 (N/R) N/R 733 (100–3000)
N/R 25–45 30–60
OEP 5 Ovarian ectopic pregnancy; N/R 5 not reported.
bleeding. Circulatory collapse was present in 1 (8%) of 12 patients in our study. However, the reported incidence of circulatory collapse varies with different studies. In 2004, the incidence of circulatory collapse was reported as 23% between 1971 and 1989 and 30% between 1990 and 2000 [21]. In a series of 8 cases, none of the patients had circulatory collapse [1]. These differences may be a reflection of how early diagnosis is made. The mean duration from the last menstrual period to diagnosis is reported to be 6 to 7.25 weeks by some of the large case series (Table 3). However, reports in the literature also exist of late diagnosis and ovarian pregnancies surviving to advanced gestation. Seki et al (1997) [22] described an ovarian pregnancy diagnosed at cesarean section performed at 30 weeks’ gestation and a different study [23] described a case of full-term ovarian pregnancy. In 1998, a case of heterotopic ovarian pregnancy proceeding to term was reported [24]. The diagnosis of ovarian pregnancy remains a challenge and many cases are still missed at ultrasonography [25]. The criteria for diagnosing ovarian pregnancy are mainly surgical and cannot be established by ultrasonography [27]. In spite of this limitation, increasingly more cases are diagnosed at ultrasonography. In 1990 authors reported 40% of their cases diagnosed preoperatively as ectopic pregnancies on ultrasonography [14]. Years later, other authors reported 75% to 100% of their cases diagnosed as ectopic gestation on ultrasonography (Table 4). However, until recently a definitive diagnosis of OEP on ultrasound scan was made in only a few cases (Table 4). The view was expressed that the difficulty in making a definitive diagnosis of OEP on ultrasonography limits the use of medical treatment as laparoscopy is usually needed for diagnosis. Our study suggests an improvement in the definitive diagnosis of ovarian pregnancy. This could be attributed to the reporting of sonographic features of OEP and increasing ultrasonography experience. A number of authors have described the presence of a ringlike echogenic structure on the surface or in the substance of the ovary [26–30]. Ultrasonographic images of ovarian ectopics were published with wide echogenic rings and small internal echolucent areas [31]. The echogenic ring was absent in the only patient with a ruptured OEP. The echogenicity of the ring was greater than the ovary in the other 5 cases. This is an important sonographic feature as a corpus luteum in
pregnancy may also have a ringlike appearance on ultrasonography. Various authors have reported the corpus luteum to be of less or equal echogenicity to the ovary in most cases whereas ectopics (tubal or ovarian) were usually more echogenic than the ovary or corpus luteum [32–34]. In our experience the ovarian ectopic was more echogenic than the surrounding ovarian tissue (Fig. 2) in keeping with the findings of these authors. The presence of a yolk sac or fetal pole in the ovary makes the diagnosis easier but these are reported to be less common findings [32]. A fetal pole was identified in only 1 (8%) of our cases. We share the view of other authors [12] that serum b-hCG measurements are a useful diagnostic tool when ultrasound scan findings are inconclusive. Ovarian ectopics were associated with low (,1000 IU/L) serum b-hCG levels [25]. This was not our experience as most of our patients had serum b-hCG levels greater than 1000 IU/L. Typically the ovarian ectopic has the appearance of a hemorrhagic ovarian mass (Fig. 3) at surgery. However, ovarian ectopics can also pose a diagnostic dilemma at surgery as they can be misdiagnosed as hemorrhagic corpus luteum or ovarian cysts. [25,26]. This is illustrated by one of our cases initially thought to be a ruptured corpus luteum and later confirmed to be an ovarian ectopic at histology. In an attempt at resolving this diagnostic dilemma, a study advised that an ovarian hemorrhagic mass associated with normal tubes, a serum concentration of hCG greater than 1000 IU/mL, and
Fig. 2. Ultrasound image of ovarian pregnancy.
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In view of concerns about future fertility, current practice is to resect the ovarian pregnancy and preserve healthy ovarian tissue. Oophorectomy is rarely indicated. Our ovarian pregnancy resection rate of 92% by laparoscopy is one of the highest in the published literature (Table 4). Trophoblastic tissue may persist after resection of the pregnancy making further treatment necessary. For this reason, follow-up hCG levels must be obtained. However, none of our patients required further treatment. It is also noteworthy that operating time was short (mean 49 minutes) and no complications occurred. Our experience with laparoscopic management of OEP reveals that it is effective, safe, and conserves ovarian function in most cases. In addition, it offers a short hospital stay, requires minimal follow-up, and allows the patient to resume normal activity within a short period of time. Fig. 3. Laparoscopic image of ovarian pregnancy.
absent intrauterine sac suggests an ovarian pregnancy [1]. This serves as a useful guide, with the main limitation being cases with hCG less than 1000 IU/L. A review of the literature on the management of ovarian pregnancy reveals that surgery is currently the mainstay of management and medical management is still less frequently performed (Table 4). The first reported case of successful medical management of OEP with methotrexate was in 1988 [34]. Subsequently, other successful cases were reported [35,36]. Medical management has the advantage of being less invasive than surgery. However, its use appears to be limited by the need to perform diagnostic laparoscopy in many cases. Many authors share the view that if laparoscopy is required for diagnosis, definitive surgical management should be performed at the same time [34]. However, cases of medical treatment performed after laparoscopy are reported [35]. We anticipate that the positive trend in the definitive diagnosis of ovarian pregnancy by ultrasonography will in future increase the proportion of cases managed medically. Increasingly, operative laparoscopy is the method of choice in the surgical management of OEP [14] since the first reported case in 1988 [6]. A review of case reports on the surgical management of ovarian ectopics reveals that operative laparoscopy was performed in 26% of cases from 1988 through 1997 and in 51% of cases from 1998 through 2008 (Fig. 1). Likewise, a review of case series indicates an increase in operative laparoscopy rate from 10% [14] to 100% in our study (Table 4). Significant hemoperitoneum was reported as a common indication to convert from laparoscopy to laparotomy [14]. However, in our experience this is no longer an absolute indication for conversion to laparotomy as illustrated in one of our cases when operative laparoscopy was performed in the presence of significant hemoperitoneum of 3000 mL (Table 2) and in other reports in literature [37], but laparoscopy under these circumstances depends on surgical expertise and adequate resuscitation of the patient.
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