Pathology International

2003;

53

: 806–809

Blackwell Science, LtdOxford, UKPINPathology International1320-54632003 Japanese Society of PathologyNovember 20035311806809Case Report

Ovarian pregnancyH. Itoh

et al.

Correspondence: Hiroshi Itoh, MD, PhD, Second Department ofPathology, Miyazaki Medical College, 5200 Kihara, Kiyotake,Miyazaki 889-1692, Japan. Email: hitoh@post.miyazaki-med.ac.jp

Received 10 April 2003. Accepted for publication 6 June 2003.

Case Report

Ovarian pregnancy: Report of four cases and review of the literature

Hiroshi Itoh,

1

Akira Ishihara,

2

Hiroyuki Koita,

2

Kinta Hatakeyama,

3

Tomoko Seguchi,

1

Yutaka Akiyama,

1

and Hiroaki Kataoka

1

1

Second and

3

First Departments of Pathology, Miyazaki Medical College and

2

Department of Pathology, Prefectural Nobeoka Hospital, Miyazaki, Japan

Ovarian ectopic pregnancy is rarely seen; it constitutes only0.5–3% of all ectopic pregnancies and the incidence is only1 for every 7000–40000 deliveries. We herein report fourcases of primary ovarian pregnancy encountered during thelast 10 years in Miyazaki prefecture, Japan. The patients inall of these cases were admitted to their local hospitals withincreased lower abdominal pain and intraperitoneal bleed-ing, and had surgery for total or partial oophorectomy.Grossly and microscopically, chorionic villi were exclu-sively found in the ovary but not in the fallopian tube, sothat we diagnosed these cases as primary ovarian pregnan-cies. None of the patients were known to have used anintrauterine contraceptive device, which have been sug-gested as the cause of ovarian pregnancies in severalstudies. The incidence of ovarian pregnancy is recentlyincreasing, and pathologists will have increased chances todiagnose this disease.

Key words:

ectopic pregnancy, intrauterine contraceptivedevice, ovarian pregnancy, ovary, pelvic inflammatory disease

Ectopic extra-uterine pregnancy is an event that concernsfrom 1/30 to 1/300 pregnancies.

1,2

Approximately 0.5–3.0%of these are ovarian pregnancies, a rare condition thatoccurs when a fertilized ovum implants itself in the ovary.

2–4

Because of the increased vascularity of the ovarian tissue,ovarian pregnancy usually results in rupture and hemoperi-toneum. Initial diagnosis is only made by histopathology onthe basis of the four Spilberg’s principles.

5

The incidence ofectopic pregnancy has been reported to have increased overthe last two decades, but to date, the actual etiology ofovarian pregnancy is not yet fully understood. Previous casereports of ovarian pregnancy are seen mainly in obstetrics

journals,

4,6–17

and only some of these describe the histo-pathological characteristics of this disease.

2,18–20

Here wereport four cases of primary ovarian pregnancy encounteredduring the last 10 years in Miyazaki prefecture, Japan, withhistological characteristics and a literature review.

CLINICAL SUMMARY

The patients’ ages were 21, 27, 33 and 36 at the onset ofdisease and all had no history of the use of intrauterinecontraception devices (IUCD) nor prior abdominal surgery.No remarkable past histories were noted, including sexuallytransmitted diseases (STD), pelvic inflammatory disease(PID), endometriosis or infertility, except for the history ofhypothyroidism in case 4. Case 3 had a past history of twonormal pregnancies and deliveries, while cases 2 and 4were their first pregnancies. They were admitted to theirlocal hospitals with increased lower abdominal pain. Theyshowed increased levels of serum

b

human chorionic gona-dotropin (

b

hCG), but no gestational sac was found in theuterus and intraperitoneal bleeding was found in all casesby ultrasound scanning. Therefore, ectopic pregnancies(cases 1, 3 and 4) or torsion of the ovary (case 2) weresuspected, and surgery for total (cases 1–3) or partialoophorectomy (case 4) was carried out. The patient’s pro-files are summarized in Table 1.

PATHOLOGICAL FINDINGS

Grossly, ovaries were swollen and ruptured in part. Hemor-rhagic tissues, including chorionic villi, were present exclu-sively in the ovaries but not in the fallopian tubes in all fourcases. The cut surface of the ovary in case 4 showed hem-orrhagic tissue surrounded by a yellowish corpus luteum(Fig. 1a). Histologically, some chorionic villi showing first tri-

Ovarian pregnancy 807

mester were observed within the cavity of the corpus luteumin case 4 (Fig. 1b) and adjacent to the ruptured region of theovary in case 3 (Fig. 1c), admixed with hemorrhagic andnecrotic tissues. Chorionic villi were also found within thecavity of the corpus luteum in cases 1 and 2 (not shown). Nodecidual change was observed in the ovarian stroma of anyof the cases. A small follicle cyst was observed in case 3,

and a large coagula was attached in the ovary of case 2,which was suggested to be the torsion of the ovary. Noapparent proliferation of atypical trophoblastic cells was seenin case 3 (Fig. 1d) or in any other case, and no ovarian orpelvic endometriosis was found. From these findings, wediagnosed all four of these cases as primary ovarianpregnancies.

Table 1

Summary of the patients’ profiles

Case YearAge

(Years)Past pregnancy/

deliveryDays after

LMPPreoperative

diagnosisSize(cm) Side

1 1993 33 Unknown Unknown Ovarian pregnancy 4

¥

3

¥

2.5 Right2 1999 21 0/0 50 Torsion of the tumor 3

¥

2

¥

2 Right3 2001 36 2/2 43 Ectopic pregnancy 3

¥

2.5

¥

2.5 Right4 2001 27 0/0 71 Ectopic pregnancy 3

¥

2.5

¥

2 Left

LMP, last menstrual phase.

Figure 1

Gross and microscopic appearances of ovarian pregnancies. (

a

) The cut surface showed hemorrhagic tissue surrounded by ayellowish corpus luteum in the ovary of case 4. (

b

) Histologically, some chorionic villi showing first trimester (arrow) were observed withinthe cavity of the corpus luteum (left side of the figure), admixed with hemorrhagic and necrotic tissues (HE). (

c

,

d

) In case 3, chorionic villi(arrow) were also observed adjacent to the corpus luteum (right side of the figure). No apparent proliferation of atypical trophoblastic cellswas seen (HE).

808 H. Itoh

et al.

DISCUSSION

Final diagnosis of primary ovarian pregnancy is made onlyby histopathology after surgery on the basis of the fourSpilberg’s principles: (i) the gestational sac must occupy thenormal position of the ovary; (ii) the tube on the side of thepregnancy must be normal; (iii) the gestational sac must beconnected to the uterus by the utero-ovarian ligament; and(iv) ovarian tissue must be histologically determined in thewall of the gestational sac.

5

However, the ovary is alreadyruptured at the time of operation in most of the cases andthe gestational sac is not easily detected in these cases.Thus, the histopathological diagnosis of ovarian pregnancyis usually made by the existence of chorionic villi restrictedwithin the ovary and not in the fallopian tube. In our cases,the gestational sac was not detected, but chorionic villi wereobserved within the cavity of the corpus luteum (cases 1, 2and 4) or adjacent to the ruptured region of the ovary (case3) but not in the fallopian tubes. These histological findingswere compatible with those of primary ovarian pregnancies,as reported previously.

2,18–20

The histopathological diagnosisof primary ovarian pregnancy is therefore not so difficult, butit must be distinguished from very rare examples of primaryovarian gestational trophoblastic disease by applying criteriasimilar to those used in the uterus.

21

In our cases, chorionicvilli were observed in the ovary and no apparent proliferationof atypical trophoblastic cells was seen (Fig. 1d), so thattrophoblastic disease could be discounted easily.

The etiology of ovarian pregnancy is obscure at present,but Boronow

et al

. summarized the possible etiologies asfollows: (i) obstructed ovulation due to inflammation such asPID and perioophoritis, tenacious discus proligerous and/orlow intrafollicular pressure; (ii) ineffective tubal ciliary and/orperistaltic function due to inflammation or idiopathy; (iii) favor-able surface phenomena such as decidual changes orendometriosis of the ovary; (iv) parthenogenesis; and (v)chance.

6

The incidence of ectopic pregnancies has beenreported to have increased over the last two decades, follow-ing a rise in the prevalence of STD, the increased number ofwomen with a history of PID and the increased use ofIUCD.

2,6–9

In contrast to patients with tubal pregnancies,many of the patients with ovarian pregnancies have a historyof PID which occurred after STD, pelvic surgery or treatmentfor infertility. PID can induce either a reduction of the tubalmotility or a thickening of the ovarian albuginea secondaryto an inflammatory response, causing an increased risk ofintrafollicular pregnancy due to a hampered follicular dehis-cence. IUCD prevents implantation in the uterus with 99.5%effectiveness and implantation in the tube with 99% effective-ness; it has no effect on ovarian implantation. However, IUCDis not a popular tool for contraception in Japanese women incontrast to women of other countries,

22

and indeed, none ofthe cases in this study has ever been known to use an IUCD.

In addition, there were several cases of ovarian pregnancythat occurred after

in vitro

fertilization, or were associatedwith a contralateral corpus luteum.

16,18–20

This suggests thatmigration of a fertilized egg to the ovary and its subsequentimplantation in the ovary is a possible process for ovarianpregnancy. In the present cases, the patients had no pasthistory of PID, endometriosis,

in vitro

fertilization or the useof IUCD, so that the cause of ovarian pregnancy might beidiopathic insufficiency of ovarian and tubal function or otherunknown reasons, such as disturbance of the hormonalbalance by environmental factors or unknown pathogenicfactors.

ACKNOWLEDGMENTS

The authors wish to thank Mr T. Miyamoto and Ms Nomurafor their skillful technical assistance.

REFERENCES

1 Wheeler JE. Diseases of the Fallopian tube. In: RJ Kurman, ed.

Blaustein’s Pathology of the Female Genital Tract

, 5th edn. NewYork: Springer-Verlag, 2002; 630–3.

2 Gaudoin MR, Coulter KL, Robins AM, Verghese A, HanrettyKP. Is the incidence of ovarian ectopic pregnancy increasing?

Eur J Obstet Gynecol Reprod Biol

1996;

70

: 141–3.3 Clement PB. Nonneoplastic lesions of the ovary. In: RJ

Kurman, ed.

Blaustein’s Pathology of the Female Genital Tract

,5th edn. New York: Springer-Verlag, 2002; 714.

4 Hallat JG. Primary ovarian pregnancy: a report of twenty-fivecases.

Am J Obstet Gynecol

1982;

143

: 55–60.5 Spiegelberg O. Zur Casuistik der Ovarialschwangerschaft.

ArchGynaekol

1878;

13

: 73–9.6 Boronow RC, McElin TW, West RH, Buckingham JC. Ovarian

pregnancy: report of four cases and thirteen-year survey of theEnglish literature.

Am J Obstet Gynecol

1965;

91

: 1095–106.7 Gray CL, Ruffolo EH. Ovarian pregnancy associated with

intrauterine contraceptive devices.

Am J Obstet Gynecol

1978;

132

: 134–9.8 Al-Meshari AA, Chowdhury N, Adelusi B. Ovarian pregnancy.

Int J Gynecol Obstet

1993;

41

: 269–72.9 Grimes HG, Nosal RA, Gallagher JC. Ovarian pregnancy. a

series of 24 cases.

Obstet Gynecol

1983;

62

: 174.10 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

: 1182–5.11 Tuncer R, Sipahi T, Erkaya S, Akar NK, Baysar NS, Ercevik S.

Primary twin ovarian pregnancy.

Int J Gynecol Obstet

1994;

46

:57–9.

12 Mall AK. Ovarian pregnancy: A case report emphasizing theneed for careful histologic review.

J Reprod Med

1996;

41

: 453–4.

13 Seki H, Kuromaki K, Takeda S, Kinoshita K. Ovarian pregnancydiagnosed in the third trimester: a case report.

J Obstet Gynae-col Res

1997;

23

: 543–6.14 Shahabuddin AKM, Chowdhury S. Primary term ovarian preg-

nancy superimposed by intrauterine pregnancy: a case report.

J Obstet Gynaecol Res

1998;

24

: 109–14.

Ovarian pregnancy 809

15 De Seta F, Baraggino E, Strazzanti C, De Santo D, TracanzanG, Guaschino S. Ovarian pregnancy: a case report.

ActaObstet Gynecol Scand

2001;

80

: 661–2.16 Oliveira FG, Abdelmassih V, Costa ALE, Balmaceda JP, Abdel-

massih S, Abdelmassih R. Rare association of ovarian implan-tation site for patients with heterotopic and with primary ectopicpregnancies after ICSI and blastocyst transfer.

Hum Reprod

2001;

16

: 2227–9.17 Suwa M, Hoshino T, Himeno K

et al.

Ovarian pregnancy: reportof two cases and survey of fifteen cases in an 11-year period.

Sanka Fujinka

1989;

56

: 1972–8 (in Japanese).18 Bontis J, Grimbizis G, Tarlatzis BC, Miliaras D, Bili H. Intrafol-

licular ovarian pregnancy after ovulation induction/intrauterineinsemination: pathophysiological aspects and diagnostic prob-lems.

Hum Reprod

1997;

12

: 376–8.

19 Shibahara H, Funabiki M, Shiotani T, Ikeda Y, Koyama K. Acase of primary ovarian pregnancy after in vitro fertilizationand embryo transfer.

J Assist Reprod Genet

1997;

14

: 63–4.

20 Toki T, Obinata M, Nakayama K, Oguchi O, Fujii S. Ovarianpregnancy associated with microscopic dicidualized endometri-osis of the ovary: report of a case.

J Obstet Gynaecol Res

1998;

24

: 45–8.21 Scully RE, Young RH, Clement PB. Tumors of the ovary, malde-

veloped gonads, fallopian tube, and broad ligament. In: J Rosai,LH Sobin, eds.

Atlas of Tumor Pathology.

Bethesda: ArmedForces Institute of Pathology, 1998; 430.

22 Fuse Y. Case study of ovarian pregnancies.

Sanfujinka NoJissai

1992;

41

: 501–507 (in Japanese).