Goran Augustin1, 2
(1)
Department of Surgery Division of Gastrointestinal Surgery, University Hospital Center Zagreb, Zagreb, Croatia
(2)
School of Medicine University of Zagreb, Zagreb, Croatia
Abstract
Follicular and corpus luteum cysts of the ovary are functional cysts and benign growths of the ovary. A follicular cyst arises from a normal follicle that fails to undergo ovulation or does not undergo the normal atretic process. It is usually clear and fluid filled. Corpus luteum cysts are less common than follicular cysts but are more associated with clinical symptoms. Ovarian cysts are not commonly found in pregnancy. Eiss, in 1930, reports a case of bilateral tumors, each of which ruptured in pregnancy. Their frequency varies with reports of different series. In Sloane Hospital (1931), the incidence was 1/500 pregnancies; in the University of California Hospital, 1/1,500, and in McKerron’s compilations (1903), it was 1/2,500 pregnancies [1]. The tumors are thought to occur more often in nonpregnant women of the same relative age for which reason some believe they interfere with conception. Most of the cysts are small; they may or may not grow rapidly during pregnancy.
14.1 Incidence
14.1.1 Ovarian Cysts
Follicular and corpus luteum cysts of the ovary are functional cysts and benign growths of the ovary. A follicular cyst arises from a normal follicle that fails to undergo ovulation or does not undergo the normal atretic process. It is usually clear and fluid filled. Corpus luteum cysts are less common than follicular cysts but are more associated with clinical symptoms. Ovarian cysts are not commonly found in pregnancy. Eiss, in 1930, reports a case of bilateral tumors, each of which ruptured in pregnancy. Their frequency varies with reports of different series. In Sloane Hospital (1931), the incidence was 1/500 pregnancies; in the University of California Hospital, 1/1,500, and in McKerron’s compilations (1903), it was 1/2,500 pregnancies [1]. The tumors are thought to occur more often in nonpregnant women of the same relative age for which reason some believe they interfere with conception. Most of the cysts are small; they may or may not grow rapidly during pregnancy.
In the first trimester of pregnancy, ovarian cysts are often functional and generally resolve without complications, and therefore these were assumed to be physiological in nature [3, 4]. These resolving cysts were classified as cystic or hemorrhagic corpus lutea based on their appearance on gray-scale ultrasound [5]. After 16 weeks’ gestation, the prevalence of ovarian cysts is 0.5–3.0 % [3, 5]. Interestingly, of the ovarian cysts that persisted at 20 weeks’ gestation, 78.6 % were present at the 6-week postnatal scan, and all of these were pathological [5]. Zanetta et al. in a recent cross-sectional study assessed the prevalence of ovarian cysts at various stages of pregnancy, i.e., in the first, second, and third trimesters [4].
Only 1.2 % (79/6,636) of the women had an ovarian cyst with a maximum diameter of >30 mm. This figure is significantly lower than 5.4 % published by Condous et al. which is probably a reflection of different population groups. The earlier in gestation a scan is performed, the more ovarian cysts, and in particular functional corpora lutea, will be detected. Borgfeldt and Andolf investigated the rate of occurrence of adnexal pathology in premenopausal women aged 25–40 years. They defined an adnexal lesion as either a simple cyst with the largest diameter of at least 25 mm or a complex cyst of any size. Adnexal lesions were found in 7.8 % of the women [6]. Being a thin-walled vascular structure, such cysts are predisposed toward rupture; hemorrhage can be the primary event, but also a previous torsion can cause the cyst to rupture [7]. Rupture of adnexal torsion during pregnancy may also occur secondary to softening of the lesion following stromal decidualization [8]. Hemorrhage in the corpus luteum is a rare complication that occurs more frequently in younger women [9], especially when associated with pregnancy [10].
14.1.2 Ovarian Teratoma
The frequency of ovarian tumors is about 1/1,000 pregnancies [2], and those which are malignant are found in about 1/15,000–1/32,000 pregnancies [3]. Mature cystic teratoma (dermoid cyst) is one of the most common benign ovarian neoplasms discovered during pregnancy (24–40 %) [35, 36]. The word teratoma is derived from the Greek word teraton, meaning monster, and was used initially by Virchow in the first edition of his book on tumors, which was published in 1863 [35]. Since mature cystic teratomas are composed of all three germ cell layers, the term “dermoid” is a misnomer. The majority of these tumors occur during the reproductive years providing further support for the germ cell theory [35]. Benign cystic teratoma (BCT) is the most common benign ovarian neoplasm comprising 10–15 % of all ovarian tumors. It occurs at all stages of life, the majority of cases being diagnosed between 20 and 30 years of age [37]. This fact makes it the most common tumor during pregnancy (22–40 % of all ovarian tumors) [37]. In pregnancy, the risk of complications increases significantly including rupture, torsion, infection, and malignant degeneration. As BCT has a tendency to remain in the confines of the true pelvis, it could lead to dystocia and obstructed labor [37].
The age shift of childbearing women could cause the changing of the histological distribution pattern. Jubb [38] reported 34 cases of primary ovarian carcinoma associated with pregnancy, with only 54 % being of epithelial type [39]. Further review of 22 additional cases reported between 1963 and 1988 revealed 27 % to be of epithelial type [40, 41]. In contrast to those previous reports, Dobashi et al. showed that the most common histological types were 80 % epithelial, 60 % invasive, and 20 % borderline tumors. Of note were the two clear cell carcinomas (20 %), which is a relatively high incidence compared to other studies outside Japan; the incidence of ovarian clear cell carcinoma in Japan is the most frequent in the world [43]. Incidence of malignancy in ovarian tumors complicating pregnancy was 2–5 %, and Jubb found only 24 authentic case reports between 1882 and 1963. The characteristic age group was 30–35 with a high incidence of nulliparity [38]. The age range in the study by Creasman et al. was 18–34, and around 50 % were primigravidas [42].
14.2 Clinical Presentation
Functional cysts of the ovary commonly do not cause pain unless the cyst is accompanied by rupture, torsion, or hemorrhage. Around 37 % of Caverly’s 73 cases never gave symptoms. If the tumor is large, it may cause pressure symptoms, varying from discomfort dyspnea, bladder irritability, etc., to actual pain. Corpus luteum cysts arise from the mature corpus luteum. They more frequently attain a larger size than the follicular cyst. Corpus luteum cysts often produce a delay in the onset of the menstrual period, and when it occurs, it may be heavy in nature (Halban’s syndrome). Because the cysts are usually larger than follicular cysts and associated with intraluminal bleeding, pain may be a common complaint. The cysts usually regress spontaneously and resolve in 4–8 weeks. Rupture of a follicular cyst may cause an acute onset of pain that is usually short-lived. Corpus luteum cysts are very vascular, and severe life-threatening hemorrhage may occur when they rupture. The combination of a delayed menstrual period, acute pain, pelvic mass, and evidence of hemoperitoneum is strongly suggestive of a ruptured corpus luteum cyst. The acute pain associated with rupture of a blood-filled corpus luteum cyst is indistinguishable from that of a ruptured ectopic pregnancy. A serum beta-human chorionic gonadotropin (βHCG) level may be helpful in distinguishing these two entities.
Jubb found that common symptoms of malignant ovarian tumors during pregnancy are excessive generalized enlargement of the abdomen and lower abdominal pain which were the common presenting symptoms. Five of Jubb’s 24 patients (21 %) presented with an acute abdomen due to complications of the carcinoma such as rupture, torsion, or strangulation [38].
McKerron collected 1,290 cases in 1903 and said that 80 % of small tumors occupying the pelvis are found only upon pelvic examinations in labor [1]. On the contrary, the diagnosis was made during pregnancy in 77 % of Caverly’s 83 cases. The absence of symptoms in one-fourth of cases shows the necessity of most careful antepartum routine examinations. The physical findings are often misleading. Hard semisolid dermoids or cystic tumors made tense by pressure may be mistaken for fibroids or vice versa. The abdominal distention with large flaccid cysts and fat abdomen may be most confusing. Ascites is common with cysts, but rarely occurs with fibroids.
Pelvic examination usually reveals diffuse pelvic tenderness, often lateralized to the side of the cyst, and a mass may be palpated. If hemorrhage is severe, it may produce abdominal distention and shock.
14.3 Diagnosis
14.3.1 Laboratory Findings
Diagnosis between hemorrhagic ovarian cyst and ectopic pregnancy is sometimes difficult. The distinction between these entities largely depends on the serum βHCG level. Assuming no intrauterine pregnancy is seen in an elevated serum βHCG level makes these findings strongly suggestive of the adnexal ring heralding an ectopic gestation, whereas a negative serum βHCG level makes a hemorrhagic ovarian cyst more likely [14].
14.3.2 Abdominal Ultrasound
If the patient is hemodynamically stable, pelvic and abdominal sonography is valuable. The diagnosis is easy if the cyst is in the pelvis, but it is often missed if the tumor is small and behind the uterus, when its presence may not be revealed until after labor. The hemorrhagic ovarian cyst exhibits a myriad of sonographic appearances. Most commonly it is depicted as a rounded hypoechoic mass containing low-level echoes, fine strands, or septations; however, other patterns are seen so frequently that the hemorrhagic ovarian cyst has been termed “the great imitator” [12, 13]. Occasionally, a hemorrhagic ovarian cyst presents as a thick echogenic wall surrounding a central rounded echolucent area – a pattern remarkably similar to that of the adnexal ring sign of an ectopic pregnancy. The identification of an intrauterine gestational sac essentially excludes the diagnosis of ectopic pregnancy and may permit expectant management even when intraperitoneal bleeding has occurred [11].
14.4 Treatment
14.4.1 Introduction
Because complications of abdominal surgery are increased in pregnancy, surgical management of ovarian cysts in pregnancy has been reconsidered [15]. Historically, pregnant women with persistent adnexal masses underwent elective removal of the masses in the second trimester [16]; this is no longer an acceptable practice in asymptomatic women, as surgical intervention, as either an emergency or after 24 weeks’ gestation, is associated with a poorer obstetric outcome [17]. Complications include spontaneous miscarriage or preterm premature rupture of membranes [15].
Growing understanding of the natural history of borderline ovarian tumors has allowed us to be more conservative in their surgical management, preserving fertility in many young women [18]. However, the natural history of such tumors is still unclear. In one study, three women were thought to have borderline lesions. This was based on the sonographic appearance and the presence of papillary projections that were nonvascular on color Doppler. Only one of these was confirmed histologically; the others were a benign cystic teratoma and a benign hemorrhagic ovarian cyst that had undergone torsion [18].
This highlights the difficulty in classifying some ovarian masses, and it is well accepted that 10 % of adnexal masses are extremely difficult to classify [19]. Despite the fact that the borderline lesions in the study by Crispens were managed surgically, there is evidence to suggest that expectant management of such ovarian cysts is an option [18]. In recent studies, this approach to such lesions was shown to be safe. After the pregnancy, these patients underwent surgery [5, 19].
14.4.2 Conservative Treatment
14.4.2.1 Observation
As only 0.13 % of women with an ovarian cyst required acute intervention during pregnancy, conclusion is that examining the ovaries at the time of a first trimester scan is of limited value. Those women requiring intervention will present with pain, while prior knowledge of the presence of a cyst may only increase anxiety even though the risk of complication is very low. If an apparently nonmalignant ovarian cyst is noted at the time of a first trimester ultrasound examination, the woman should be offered a follow-up scan 6 weeks after the pregnancy has concluded. Although there are no randomized clinical trials to determine the optimal management of an adnexal mass in pregnancy, experience suggests that expectant management is safe and without serious adverse outcome for both mother and fetus [4, 5].
In emergent settings, if a provisional diagnosis of hemorrhagic corpus luteum cyst with minimal hemoperitoneum can be made, most such cases may be best served by expectant management with serial clinical examination and hemoglobin measurements [9].
14.4.2.2 Aspiration
Aspiration of simple ovarian cysts during pregnancy is safe and may prevent the need for surgical intervention; in some cases, this will be the definitive treatment [20]. Neither anesthesia nor analgesia is required for such intervention. Ultrasound-guided aspiration for the relief of pain generated by simple ovarian cysts in nonpregnant women can be performed either transvaginally or transabdominally depending on the location of the cyst [21]. After 14 weeks’ gestation, the uterus is an abdominal organ, and as a result the ovaries are more easily targeted transabdominally. If the pain persists after the procedure without other symptoms or complications, a laparoscopic ovarian cystectomy after delivery is indicated [5]. Fine-needle aspiration is not appropriate if the cyst has any suspicious morphological features. It is not a common diagnostic problem because the frequency of ovarian cancer in pregnancy is reported to be 1/15,000–1/32,000 pregnancies [3].
14.4.3 Operative Treatment
If the patient is hemodynamically unstable or the diagnosis is in question, exploratory surgery is required. In hemodynamically unstable patient, emergency laparotomy, not laparoscopy, is indicated because definitive surgery is mandatory in the shortest possible time period. If rupture and bleeding do occur, diagnostic and therapeutic laparoscopy is appropriate.
If a provisional diagnosis of hemorrhagic corpus luteum cyst with minimal hemoperitoneum can be made, most such cases may be best served by expectant management [9]. However, once massive hemorrhage from ruptured corpus luteum cysts occurs, it can be a life-threatening condition that requires emergent surgical intervention [10]. With advances in laparoscopic surgical procedures and the development of surgical equipment, laparoscopic treatment of a ruptured corpus luteum cyst with hemoperitoneum is highly desirable [22–25]. Further, utilizing intraoperative autologous blood transfusion, transfusion of bank blood can be avoided even in cases of massive hemoperitoneum due to ruptured corpus luteum cyst in patients with ectopic pregnancy [23, 25].
14.4.3.1 Laparoscopy
Introduction
Laparoscopic cystectomy in pregnancy was first reported in 1991 by Nezhat et al. [26] and then a second case in 1994 by Howard and Vill [27]. Since then, for various reasons, laparoscopic surgery in pregnancy has rapidly increased as surgeons realized the safety of the technique in general as well as in pregnancy. Pregnancy is no longer considered as an absolute contraindication for laparoscopic procedures. There is evidence to suggest that laparoscopy and laparotomy do not differ with regard to fetal outcome, that is, fetal weight, gestational age, growth restriction, infant survival, and fetal malformations [31]. However, the major advantages of laparoscopy are magnification and panoramic view of the pelvis resulting in reduced intraoperative uterine manipulation which may lead to decreased postoperative uterine irritability, miscarriage rate, and preterm labor which is seen in 50 % of third trimester cases with an open approach. In addition, the cosmetic results are much better, and the discomfort of stretching and distension of the laparotomy scar due to the rapidly growing uterus is avoided. Very few case series provide long-term follow-up. Only one series with 11 cases of 1–8 years of follow-up has reported no evidence of developmental or physical abnormalities in the resultant children after acute non-obstetrical surgery during pregnancy [32].
With increasing gestational age, the uterus rises out of the pelvis, and there is an increasing chance of injury while inserting the Veress needle. Generally, open cannulation laparoscopy or Palmer’s point entry is recommended for laparoscopy during pregnancy. This avoids the risk of penetrating injury to the pregnant uterus by either the Veress needle or the trocar cannula [28].
Cystectomy
After confirmation that the bleeding is secondary to a cyst, conservative therapy consisting of removing the cyst and coagulating its base is standard therapy. If it is necessary to remove a corpus luteum of early pregnancy (prior to 12 weeks), progesterone replacement is advisable following surgery.
Large cystic masses may require decompression to fit though a small incision. By decompressing a cyst into a laparoscopic bag, spillage can be minimal or nonexistent. Copious irrigation also helps to keep the residual content to a minimum [29]. After cystectomy, the ovarian incision can be left open or approximated by three techniques:
· Fine monofilament suture of the edges
· Tissue glue
· Coagulation of the ovarian cortex adjacent to the surface, which will in some instances evert the edges
Stitching is necessary to avoid adhesions between the raw ovarian surface and the raw peritoneal surface left after bowel adhesiolysis in the left adnexa [29].
Furthermore, the risk of obstruction of labor by ovarian cyst or tumor is calculated to be 17–21 % [30]. Antenatal operative procedures ranging from aspiration of the cyst to oophorectomy are described in the literature to prevent the risk of obstruction of labor.
14.4.3.2 Bilateral Ovariectomy/Adnexectomy
There are many reported cases where both ovaries have been removed and the pregnancy has normally continued. It is usually stated that the corpus luteum is indispensable to pregnancy for the first two months and removal during that time precipitates abortion. Waldstein, however, recently removed bilateral dermoids at the second month without interrupting the pregnancy. Caverly reports two abortions following eight single ovariotomies before the third month of pregnancy. Another two patients continued early pregnancy to term after bilateral ovariectomy. Both women, however, had many children [33].
14.4.3.3 Ovarian Teratoma
Elective
Treatment of suspected ovarian teratoma is surgical removal as soon as possible after diagnosis to avoid complications. They may be responsible for torsion, rupture, and obstruction during labor. Rupture is rare, but once it has occurred, it can cause complications such as chemical or granulomatous peritonitis mimicking advanced ovarian malignancy [37, 44, 45].
All efforts should be made to avoid rupture or leakage of cyst fluid during the operation. If it happens before or during the operation, copious saline washing should be performed to minimize chemical peritonitis and its sequel [44, 46, 47]. When BCT is found incidentally in the first trimester of pregnancy, surgical removal should be performed at 14–16 weeks of gestation to avoid the risk of damage to the corpus luteum. If diagnosis of BCT occurs at 16–22 weeks, surgery should be performed as soon as possible. If it is first discovered after 22 weeks of pregnancy, the treatment may be deferred until delivery [37]. Over 200 cases of BCT in pregnancy have been reported in the literature, and many of them ruptured spontaneously or iatrogenically. In a review of 47 cases, Kocak et al. reported that during cyst extraction, minimal spillage occurred in 42.5 % of cases and none developed chemical peritonitis [48]. Clement et al. [46] and Achtari et al. [47] reported chemical peritonitis following cystic fluid spillage. The patients needed further surgeries to treat the complications. Two other case reports by Suprasert et al. [37] and Phupong et al. [45] reported a diffuse peritoneal reaction mimicking advanced ovarian malignancy where full surgical staging was performed. Postoperative histological examination revealed BCT and chronic granulomatous peritonitis. A conservative approach was adopted, and patients were free of symptoms without further treatment at 12 months [36, 45]. The incidence of chemical peritonitis after rupture and leakage of cystic fluid in the peritoneum is less than 0.5 % [35]. The incidence of chronic granulomatous peritonitis after rupture or leakage of cystic fluid is also extremely rare. In granulomatous peritonitis after ruptured ovarian teratomas, numerous nodules of mature glial tissue implant on a widespread area of the peritoneum [49].
Emergent
Ruptured BCT of the ovary mimicking gynecological malignancy is uncommon and could be misdiagnosed [45]. Intra-abdominal peritoneal seedlings, adhesions, and/or masses are frequent sequel. In most such cases, abdominal seedlings are essentially of mature neuroglial elements, and long-term survival rate is good. Recognition of a dermoid tumor associated with glial seedling is important to avoid unnecessary debulking surgery. Following postoperative adhesions, fibrous bands, or obstructions, conservative management seems to have a good prognosis.
14.5 Prognosis
14.5.1 Maternal Outcome
14.5.1.1 Continuation of Pregnancy
There are several possible pathophysiologic mechanisms that can interfere with normal continuation of pregnancy. First is hormonal influence. The problem could arise if bilateral adnexectomy/ovariectomy is performed. Fortunately, there are cases with normal further pregnancy after that procedure (see Sect. 14.4). Second is obstruction of labor or pregnancy with the tumor or uterus incarcerated in the pelvis. The third is secondary infection of primary ovarian pathology. Graefe stated that ovarian cysts produce abortions or premature labor in 14–20 % of cases.
14.5.1.2 Malignant Tumors
In 21 of the reviewed cases by Jubb, the diagnosis was followed by immediate laparotomy and unilateral oophorectomy. Fourteen of these patients had no further treatment. In the 33 % (7/21) of reexplored patients, no residual carcinoma was found. Unfortunately, there is no record of grading of the carcinoma, and follow-up was inadequate. Because of this, the figure for the 5-year survival rate of nearly 60 % is unreliable [38]. All of Creasman et al.’s more radically treated patients with stage IA ovarian carcinoma were well at 5 years, and they claimed that this demonstrated the value of a more radical approach to treatment. It would seem equally likely that the good survival rates reflected early diagnosis at routine antenatal examinations of patients. It is obvious that sacrifice of the pregnancy does not improve the maternal prognosis and that unilateral oophorectomy can be employed [42].
14.5.2 Fetal Outcome
Even with therapeutic interventions, fetal mortality remains high at 31 % for significant nontraumatic intraperitoneal bleeding [34].
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