Shivamurthy and Gurumurthy: A clinicopathological study of ovarian endometriotic cysts


Introduction

Endometriosis is an important gynecologic disorder with multifactorial causes, primarily affecting women during their reproductive years. It usually affects premenopausal females.1, 2 Pathologically, endometriosis refers to the presence of functioning endometrial glands and stroma outside the uterine cavity, which may vary from microscopic endometriotic implants to large cysts.2, 3, 4 The various sites where these can be found include both the ovaries, the pouch of Douglas, pelvic peritoneum and uterosacral ligaments.4, 5 Clinically patients may be asymptomatic or may present with disabling pelvic pain, infertility, or adnexal masses.1, 5, 6 Occasionally these can enlarge to present as huge abdominal masses which can mimic ovarian malignancy. Cyst aspiration, fenestration and ablation of cyst wall are some the commonly performed surgical procedures.7, 8

Materials and Methods

A total of 35 patients who underwent ovarian cystectomy for endometriotic cysts between January 2019 and December 2020 were retrospectively identified. The clinical findings, gross and histopathological features were noted in each case. Microscopically, all the histopathological features were noted and the presence or absence of ovarian tissue adjacent to the cyst wall was evaluated. If ovarian tissue was present, the morphologic characteristics were graded on a semi-quantitative scale of 0-4 as described by Muzii et al.4 Grade 0: complete absence of follicles; Grade 1: primordial follicles only; Grade 2: primordial and primary follicles; Grade 3: some secondary follicles; Grade 4: pattern of primary and secondary follicles as seen in the normal ovary.

Results

The age group of patients ranged between 22-28yrs. Right side cysts accounted for the majority, however 6 cases had bilateral endometriotic cysts.

Clinically patients presented with primary infertility, pain abdomen, dysmenorrhea and dyspareunia. A combination of these clinical features were frequently found. However those with primary infertility accounted for the majority accounting for 46.2%.

Table 1

Graph showing the various clinical features

Clinical feature

Percentage

Primary infertility

46.2%

Pain abdomen

38%

Dysmenorrhoea

42.8%

Dyspareunia

32%

On gross morphological examination, the maximum weight recorded for these cysts was 35gm. The size of the lesions ranged from 4.5 to 18cm with the median thickness of the cyst wall being 0.7cm. More than 80% of the cases presented as cystic lesions filled with chocolate coloured thick fluid.

Table 2

Gross morphological features of the cysts analysed

Gross Morphological Features

Weight range

5gm

35gm

Size

4.5cm

18cm

Median wall thickness

0.7cm

On analysis of the various histopathological features, the lining epithelium was identified in about 68% of cases, few showing atypia and oncocytic change. (3.9% and 4.3%). Fibrosis and hemosiderin laden macrophages were present in 72.6% and 80.6% of cases respectively. Endometrial glands and stroma were present in 53.2% and 61% cases respectively. Inflammation when present was predominantly lymphocytic. [Figure 1, Figure 2, Figure 3, Figure 4, Figure 5, Figure 6]

Table 3

Histopathological features of endometriotic cysts analysed

Features analysed

Present (%)

Lining Epithelium

68%

Present with atypia

3.9%

Oncocytic change

4.3%

Fibrosis

72.6%

Adjacent endometrial glands

53.2%

Endometrial stroma

61%

Hemosiderin laden macrophages

80.6%

Ceroid laden macrophages

6.8%

Inflammatory Component

Lymphocytes

59.2%

Plasma cells

43%

Esosinophils

2.3%

Neutrophils

5.5%

Histiocytes

96.7%

On evaluation of the ovarian tissue, 42.8% of cases showed no follicles and the rest showing grades ranging from 1 to 4, with grade 1 accounting for majority.

Table 4

Grading of adjacent ovarian tissue in endometriotic cysts

Grade

No of cases (Frequency)

Percentage

0

15

42.8

1

8

22.8

2

4

11.5

3

6

17.2

4

2

5.7

Total

35

100

Figure 1

Endometrial cyst wall with eroded lining epithelium and areas of hemorrhage [H&Ex40]

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/77e67088-7fb0-406e-9c41-48ba7e9ccbe5/image/66474f26-914e-4eeb-98b3-1bd410f72d6e-uimage.png

Figure 2

Cyst wall with the presence of lining epithelium [H&Ex400]

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/77e67088-7fb0-406e-9c41-48ba7e9ccbe5/image/3e7c8fbb-7660-468e-b657-282c6aec8ebf-uimage.png

Figure 3

Cyst wall with hemosiderin laden macrophages [H&Ex200]

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/77e67088-7fb0-406e-9c41-48ba7e9ccbe5/image/eff52a71-7909-42df-b9a6-d97a1e59b402-uimage.png

Figure 4

Cyst wall with endometrial glands [H&Ex200]

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/77e67088-7fb0-406e-9c41-48ba7e9ccbe5/image/2f923f10-7ffe-4360-b176-ff7e268e3e4f-uimage.png

Figure 5

Cyst wall with endometrial stroma [H&Ex200]

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/77e67088-7fb0-406e-9c41-48ba7e9ccbe5/image/d828032e-ff65-4e02-af6a-474aa5d879c3-uimage.png

Figure 6

Adjacent ovarian stroma with primodial follicles [H&Ex200]

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/77e67088-7fb0-406e-9c41-48ba7e9ccbe5/image/ca810467-182c-4666-9ced-338e71839e2f-uimage.png

Discussion

In 1957 Hughesdon demonstrated that 93% of ovarian endometriotic cysts are formed by invagination of the cortex after the accumulation of menstrual debris from endometriotic implants.1, 6, 9 However in 1997 Nisolle and Donnez suggested that coelomic metaplasia of the invaginated epithelial inclusion is responsible. Scurry J et al. in 2001 has described the various types of ovarian endometriotic cysts.3, 4, 10 [Table 5]

Table 5

Pathogenetic types of endometriotic cysts.

Cortical invagination cysts

Surface inclusion cyst-related endometriotic cysts

Physiological cyst-related endometriotic cysts

They arise when surface ovarian endometriotic deposits adhere to another structure (such as the broad ligament) There is block in the egress of menstrual fluid produced by cyclical endometriosis Hence the fluid collects and causes the ovarian cortex to invaginate

These develop when endometriotic tissue colonizes preexisting inclusion cysts

Occur when endometriosis gains access to a follicle, such as at the time of ovulation

[i] Different pathogenetic types of ovarian endometriotic cysts.. (Scurry J et al 20013)

In the present study, majority of patients presented with primary infertility, accounting for 46.2%. Several authors have described various biological mechanisms that link infertility and endometriosis. Endometriosis can cause pelvic adhesions which can alter ovum release from the ovary. Many studies have demonstrated altered peritoneal function in patients with endometriosis. These patients have often found to have increased peritoneal fluid levels of prostaglandins, tumor necrosis factors and interleukin-1 which in turn can affect the oocyte, sperm, embryo development and function of the fallopian tube. Increase Ig A and Ig G antibody levels along with increase in lymphocytes in patients with endometriosis can affect endometrial receptivity and implantation. 3, 6, 7

On gross morphological examination, the size of the lesions in the present study ranged from 4.5 to 18cm and majority of the cases where cystic lesions. Other studies have described endometriosis to appear as “powder burn” or “gunshot” lesions on the ovaries. They may even occur as black, brown-black, or bluish shrunken lesions, nodules, vesicles or tiny cysts containing hemorrhagic material surrounded by grey white areas of fibrosis. A few cystic lesions may be adherent to the peritoneum and adjacent fallopian tubes forming tubo-ovarian masses.1, 3, 10

On microscopic examination, 68% cases showed cyst wall composed of endometrial lining with a majority of cases showing fibrosis [72.6%] and hemosiderin laden macrophages[80.6%]. Endometrial glands and stroma were present in 53.2% and 61% cases respectively. The diagnosis of endometriosis on histopathology is often straightforward in those cases where endometrial-type glands and stroma are present. However the diagnosis is often challenging in cases where the endometrial stroma is very scant and when there is extensive fibrosis. The three different types of stroma i.e. fibrous stroma, ovarian stroma, and endometrial stroma may be difficult to distinguish. In such cases multiple serial sections need to be examined. CD10 immunohistochemistry can be of additional value in diagnosing endometriosis in difficult cases where CD10 stains the endometrial stroma.4, 5, 8, 11

Majority of cases in the present study showed the absence of follicles with the presence of primordial follicles in 22% of cases. These findings suggest that the capsule is the invaginated cortex itself and hence their removal affects the ovarian stroma. Thus excision of endometriotic cyst wall may cause loss of functional ovarian tissue. This is of paramount importance in surgical treatment of infertility in patients presenting with endometriosis. Thus ovarian endometriomas could thus affect the response to ovarian stimulation, oocyte recovery, implantation and fertilization rates.8, 9

In relation to the treatment aspect, several authors suggest that laproscopic treatment of ovarian endometriotic cysts should consist of drainage & coagulation rather than excision. Controversy still exists regarding the recurrence and pregnancy rates after the two procedures. Few authors suggest that in patients with bilateral endometriosis, fertility preservation with oocyte or ovarian tissue cryopreservation may be considered as a treatment option.2, 9, 11

Conclusion

The present study further emphasizes endometriosis to be an important cause of primary infertility which needs to be recognized and treated appropriately. Recognition of these cysts on histopathological examination can be challenging at times when endometrial stroma is scant and in cases of tubo-ovarian masses where these lesions could mimic malignancy. Excision of endometriotic cyst wall may cause loss of functional ovarian tissue which is extremely important in surgical treatment of infertility in patients presenting with endometriosis. This could in turn affect recovery of oocytes, implantation and fertilization rates.

Source of Funding

None.

Conflict of Interest

The authors declare that there is no conflict of interest.

References

1 

J Scurry J Whitehead M Healey Classification of Ovarian Endometriotic CystsInt J Gynecol Pathol20012021475410.1097/00004347-200104000-00006

2 

C Wellbery Diagnosis and treatment of endometriosisAm Fam Physician199960175368

3 

SC Modesitt G Tortolero-Luna JB Robinson DM Gershenson JK Wolf Ovarian and extraovarian endometriosis-associated cancerObstet Gynecol2002100478895

4 

L Muzii C Achilli F Lecce A Bianchi S Franceschetti C Marchetti Second surgery for recurrent endometriomas is more harmful to healthy ovarian tissue and ovarian reserve than first surgeryFertil Steril201510337384310.1016/j.fertnstert.2014.12.101

5 

NC Llarena T Falcone RL Flyckt Fertility Preservation in Women With EndometriosisClin Med Insights: Reprod Health20191310.1177/1179558119873386

6 

XY Li XP Chao JH Leng W Zhang JJ Zhang Y Dai Risk factors for postoperative recurrence of ovarian endometriosis: long-term follow-up of 358 womenJ Ovarian Res20191217910.1186/s13048-019-0552-y

7 

Y Liang X Yang Y Lan L Lei Y Li S Wang Effect of Endometrioma cystectomy on cytokines of follicular fluid and IVF outcomesJ Ovarian Res20191219810.1186/s13048-019-0572-7

8 

G Bedoschi V Turan K Oktay Fertility preservation options in women with endometriosisMinerva Ginecol201365299103

9 

A Aflatoonian N Tabibnejad Aspiration versus retention ultrasound-guided ethanol sclerotherapy for treating endometrioma: A retrospective cross-sectional studyInt J Reprod BioMed2020181110.18502/ijrm.v13i11.7960

10 

F Nezhat C Nezhat CJ Allan DA Metzger DL Sears Clinical and histologic classification of endometriomas. Implications for a mechanism of pathogenesisJ Reprod Med19923797716

11 

H Egger P Weigmann Clinical and surgical aspects of ovarian endometriotic cystsArch Gynecol19822331374510.1007/bf02110677



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Article History

Received : 22-06-2021

Accepted : 30-06-2021

Available online : 13-08-2021


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Article DOI

https://doi.org/10.18231/j.ijpo.2021.074


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