Hepatic Endometriosis: Systematic Review of Literature AND A … · 2018-10-02 · Global Scientific Research Journal of Surgery Page 2 Hepatic Endometriosis: Systematic Review of

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Hepatic Endometriosis: Systematic Review of Literature AND A Case Report


Laura Mastrangelo1*, Michele Masetti1, Maria Grazia De Blasiis1, Paolo Emilio Orlandi2, Angela Salerno3, Dario de Biase4, Sirio Fiorino5 and Elio Jovine1

1Department of Surgery, Maggiore Hospital, Bologna, Italy.2Department of Radiology, Maggiore Hospital, Bologna, Italy.

3Department of Anatomic Pathology, Maggiore Hospital, Bologna, Italy.4Department of Pharmacy and Biotechnology (FaBit), University of Bologna, Bologna, Italy.

5Department of Medicine, Maggiore Hospital, Bologna, Italy.

1*[email protected]

AbstractIntroduction: Endometriosis represents a very frequent condition in human pathology, in its predominant pelvic localization, however unusual sites may be affected, including liver. Hepatic Endometriosis (HE) is a diagnostic challenge, depending on the absence of specific clinical-, laboratoristic-and radiological patterns. These reasons make it difficult to diagnose this disorder preoperatively. Since a case of liver endometriosis was taken to our attention, we had the aim to review the available literature, to synthesize current knowledge on this topic and the case history of patients, described up to now.

Methods: A systematic computer-based search of published articles, according to the Preferred Reporting Items for Systematic reviews and Meta-Analysis (PRISMA) Statement was performed, and the following MESH (Medical Subject Headings) terms and keywords were used: ‘hepatic and liver endometriosis’, ‘hepatic and liver endometrioma’.

Review: We carried out a systematic search. We found 800 citations and 766 were excluded after a preliminary review of the titles and/or abstracts. Therefore, we examined the remaining 34 articles and reviewed the patients’ characteristics, described in these papers. Forty-one patients with HE (age ranging from 21 to 73 years) were included. Some of these subjects had a lesion with a diameter of more than 10 centimeters (cm). Five women presented areas of malignant transformation, arising in HE. We also described an illustrative case report.

Conclusion: HE should be included in the differential diagnosis for a woman of any age presenting with hepatic cystic or solid lesions of unknown cause, with or without a history of pelvic endometriosis.

Keywords: Endometriosis, Liver, Diagnosis, review

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IntroductionInitially described by von Rokitansky in 1860, en-dometriosis is defined as the presence of endome-trial glands and stroma outside the uterine cavity [1]. These ectopic endometrial implants are most com-monly found in the pelvis, including the ovaries, pelvic peritoneum, uterosacral ligaments, anterior and poste-

rior cul-de-sac, uterus, and fallopian tubes [2, 3]. How-ever, endometriosis can be found nearly anywhere in the body. Less common sites of involvement include the cervix, bladder, bowel, and pleural and pericardial cavities [4-10].

This case report describes a patient who initially un-derwent work up for a suspected spontaneous bleed-



ing or rupture of liver hemangiomas which was discov-ered to be hepatic endometriosis by frozen section. In addition, a review of current literature was performed, summarizing radiographic and clinical findings asso-ciated with liver endometriosis [6, 9-11] and on the pathogenesis of this pathological condition [12-14].

Literature ReviewA systematic computer-based search of published articles, according to the Preferred Reporting Items for Systematic reviews and Meta-Analysis (PRISMA) Statement, issued in 2009 [15], was conducted through Ovid interface, in order to identify relevant studies on the hepatic endometriosis. The literature review was performed in March 2018. The following electronic da-tabases were used: MEDLINE (1950 to March 2018) and the Cochrane Library (until the fourth quarter of 2017) for all relevant articles. The search strategy and the search terms were developed with the sup-port of a professional research librarian. The search text words were identified by means of a controlled vocabulary, such as the National Library of Medicine’s MESH (Medical Subject Headings) and Keywords. The used MESH terms and keywords were: ‘hepatic and liver endometriosis’, ‘hepatic and liver endome-trioma’. The inclusion criteria for our search were: 1) study designs by considering data from all published

case series, case-control-, or case reports, as well as cohort-studies; 2) articles which were reported in Eng-lish, as peer-reviewed, full-text publications. Papers published in a language other than English were ex-cluded. The PubMed ‘related articles’ features and the reference lists of retrieved articles were also searched to find additional pertinent studies. Two authors (A.S. and S.F.), independently and in parallel, performed the literature search and screened relevant articles, based on title or abstract. The accuracy of data col-lection was checked by a third reviewer P.O. and disa-greements concerning the results were settled by con-sensus between all authors. If a study was considered potentially eligible by either of the two reviewers, the full-text of this study was further evaluated. Full-text assessment was performed according to eligibility cri-teria developed to systematically include studies into this review. Our search identified 800 citations and 763 were excluded after a preliminary review of the titles and/or abstracts. Further three reports were not considered, since they were published in a language other than English. The full-text of the remaining 34 articles was retrieved for a more detailed assessment.

A flow-chart of the study search and selection pro-cess, evaluating publications on liver endometriosis available in literature, is reported in Table 1.

Table 1: Flow-Chart of the Study Search and Selection Process, Evaluating Publications on Liver Endo-metriosis Available in Literature

Hepatic endometrioma: n= 99

Hepatic endometriosis: n= 97

Liver endometrioma: n= 303

Liver endometriosis: n= 301

Articles considered, n = 34

Articles excluded, n = 766

Hepatic endometrioma: n= 99Hepatic endometriosis: n= 97Liver endometrioma: n= 303Liver endometriosis: n= 301

Articles excluded: n= 766

Articles considered: n= 34



Table 2: Features of Reported Cases of Hepatic Endometriosis

Author/Year Refer-ence

Hystory of Endome-

triosis

Coexisting pelvic endome-

triosis

Previous Pelvic operation Pathology Treatment

Finkel 1986 [11] No Not available Fallopian tube cyst removal

Hepatic endome-trioma

Cyst enucleation by laparotomy

Grabb/1986 [23] No No Fallopian tube cyst removal


Danazol + deroof-ing therapy

Rovati/1990 [38] No Yes No Hepatic endome-trioma

Left lateral seg-mentectomy by

laparotomy

Verbeke/1996 [43] No No No Hepatic endome-trioma

Hemihepatectomy by laparotomy

(2 patients included) No No No Hepatic endome-trioma

Segmental liver resection by lapa-

rotomy

Cravello/1996 [21] Yes No No Hepatic endome-triosis

Tumorectomy by laparotomy

Chung/1998 [20] Yes YesLeft ovarian

cystectomy due to endometriosis


Cyst enucleation by laparotomy

Weinfeld/1998 [44] Yes No

Total abdominal hysterectomy,

bilateral salpingo-oophorectomy

Adenosquamous carcinoma arising

in hepatic endome-triosis


rotomy

Inal/2000 [29] Yes Yes Treatment of pelvic endometriosis

Hepatic endome-triosis Danazol therapy

N’Senda/2000 [34] Yes No



Adenosarcoma arising in hepatic

endometriosis


rotomy

Bohra/2001 [17] Yes Not available





rotomy

Jeanes/2002 [30] Yes Not available




Removal of cyst by laparotomy

Huang/2002 [28] Yes Not available




Left hepatic lobectomy by lapa-

rotomy

Khan/2002 [32] Yes Not available



Hepatic endome-triosis

En bloc removal of right lobe mass, left lobe mass left

by laparotomy



Table 2 (Cont.)


Hystory of Endome-

triosis


triosis

Previous Pelvic operation

Pathology Treatment

(2 patients includ-ed) Yes No Removal of ruptured

cystEndometrial stro-

mal sarcomaRight hepatectomy

by laparotomy

Groves/2003 [24] Not available Not available

Total abdominal hys-terectomy, bilateral salpingo-oophorec-

tomy


Right hemiepa-tectomy by lapa-

rotomy

Tuech/2003 [42] No No No Hepatic endome-trioma

Removal of cyst by laparotomy

Reid/2003 [35] Yes Not available

Endometriosis surgery, subto-

tal hysterectomy, bilateral oopherec-

tomy, resection of an endometriotic bowel lesion, removal of

right lobe cyst

Hepatic endome-trioma showing

moderately atipica complex hyperpla-

sia

Right hemihepa-tectomy by lapa-

rotomy

Jelovsek/2004 [31] Yes Not availableHysterectomy with

bilateral salpingooo-phrectomy

Endometrioma with focal areas of mullerian adeno-

sarcoma

Resection of the liver mass

Nezhat/2005 [13] Yes Yes No Hepatic endome-triosis

Cyst enucleation by laparoscopi

(2 patients includ-ed) Yes Yes Treatment of pelvic

endometriosisHepatic edome-

triosisLaparoscopic exci-

sion

Sanchez-Per-ez/2006 [39] Yes Not available Ovarian cystectomy

Hepatic endome-trioma showing

moderately atipica complex hyper-

plasia with foci of carcinoma in situ

Right hepatectomy

Goldsmith/2009 [6] Yes Not available

Total abdominal hys-terectomy, bilateral salpingo-oophorec-

tomy


No anatomical resection

Asran/2010 [16] Yes Yes

Hysterectomy, right salpingo-oophorec-

tomy, bowel loop resection due to

obstruction

Hepatic endome-triosis, with involve-

ment of multiple liver segments

Not reported

Roesch-Di-etlen/2011 [37] No No No

Hepatic endometri-osis with right liver lobe involvement

Medical treatment (Danazol)

Schuld/2011 [40] No No No Hepatic endome-triosis

Atipical liver resec-tion of VIII segment



Table 2 (Cont.)


Hystory of Endome-

triosis


triosis


Fluegen/2013 [22] No No No Hepatic endome-triosis

Ultrasonic pericis-tectomy (segments

IV-V and VIII)

Hertel/2013 [26] No No Partial Hysterecto-my, oophorectomy


Resection of a large cystic hepatic lesion involving the

segments V, VI, VII, and VIII of the

liver

Bouras/2013 [18] No No No Hepatic endome-triosis

Left lateral hepa-tectomy with partial right ventricle free wall resection and medial diaphragm

resection

Rivkine/2013 [36] No No Conservative hyster-ectomy


Left lobectomy with diaphragm resec-

tion for a large cystic tumor in liver segments II and III

Hsu/2014 [27]

NA Yes Hysterectomy Hepatic endome-triosis

Follow-up every 6 months

NA Yes None Hepatic endome-triosis

Left lobe hepatec-tomy, VIII

NA None Hysterectomy Hepatic endome-triosis

Left lobe hepatec-tomy

NA YesHysterectomy +

salpingo-oophorec-tomy


Left lobe hepatec-tomy

(5 patients includ-ed) NA Yes

Hysterectomy + salpingo-oophorec-

tomy


Lesion removal, segment VI

Cantos Pal-larés/2014 [19] No Yes No Hepatic endome-

triosis

Resection of lesion in liver segment V, adhered to the right

hemidiafragm

Zhao/2014 [45] No No No Hepatic endome-triosis

Resection of a cystic mass in seg-ment IV of the liver

Liu/2015 [33] No No No Hepatic endome-triosis

Pericistectomy of a large cystic tumor

occupying segment III of the liver



Table 2 (Cont.)


Hystory of Endome-

triosis


triosis


Sopha/2015 [41] No No Right salpingo-oo-phorectomy


Laparoscopic excisional biopsy

of VII segment. No treatment, patient

in follow-up

Sherif/2016 [46] Yes YesTotal abdominal hysterectomy for

endometrosis


Hepatic segmen-tectomy of VII

segment

De Riggi/2016 [47] No No No Cystic hepatic endometriosis

Atypical left hepa-tectomy tailored

on right margins of lesion

Mastrangelo/2018 present case No No No Hepatic endome-

triosis Right hepatectomy

The first case of intraparenchymal endometriosis of the liver was reported by Finkel et al. in 1986 in a 21 years old woman, who suffered from epigastric pain, nausea, and vomiting. She was found to have an en-dometrial cyst measuring 13 cm in diameter located in the left lobe of the liver [11]. Subsequently, 40 ad-ditional cases have been reported in 33 studies [6, 14, 16-47]. Four of these reports included more than one patient [14, 27, 32, 36]. The major clinical fea-tures of these previously described 41 patients, and the present one, are summarised in Table 2. They occurred in women with an age range from 21 to 73 years. They were cystic and located either in the left or the right lobe of the liver. In some cases [6, 11, 18, 22-24, 26, 30, 34, 35, 38, 42, 43, 47], the tumours had a diameter of more than 10 cm. They most often presented with abdominal pain, which was not asso-ciated with menses. Twelve patients [14, 16, 19, 20, 27, 29, 38, 46] had a coexisting and 18 had a past history of pelvic endometriosis [6, 14, 16, 17, 20, 21, 28-32, 34, 35, 39, 44, 46]. Twenty-six of them had previously undergone pelvic surgery [6, 11, 14, 16, 17, 20, 23, 24, 27-32, 34-36, 39, 41, 44, 46]. All pa-tients with hepatic endometriosis, but three [23, 29, 37] who were treated with Danazol, underwent sur-gery. In 5 women, areas of epithelial or stromal ma-lignant transformation, arising in hepatic endometrio-sis, were observed in the resected tissue specimens (one case of adenosquamous carcinoma, 2 cases of adenosarcoma, one case of endometrial stromal sar-

coma, one case including foci of carcinoma in situ in hepatic endometrioma with atypical complex hyper-plasia) [31, 32, 34, 39, 44]. The described subjects presented both intraparenchymal and extraparen-chymal hepatic endometriosis. Further three reports were not considered, since they were published in a language other than English (one in French, one in Spanish and one in Japanese) [39, 48, 49].

Case ReportThis is a 36 years old multiparous white Caucasian woman, who was referred to our Unit in September 2010, because of acute right upper quadrant pain. The patient’s past medical history was significant for hypertension and hyperlipidemia and she had no his-tory of endometriosis. Examination revealed slight right upper quadrant tenderness, but the patient large body habitus precluded any accurate assessment for an abdominal mass. Workup revealed a dropping of hemoglobin level and the alteration of the liver func-tion tests. A dedicated abdominal ultrasound dem-onstrated a right lobe non-homogeneous liver pa-renchyma. In light of this, a Computed Tomography (CT) scan of the abdomen and pelvis was performed confirming the liver lesion and showing an iperdense area with small arterial blushes on the VI segment, in the V segment a disomogeneous lesion (5 X 4 cm), with a hypodense margin, was found. These features suggested the existence of a possible adenoma with



intralesional bleeding (Figure 1). Angiography did not reveal contrast enhancement blush compatible with active arterial bleeding. For an adequate clinical monitoring, the patient was transferred to the Inten-sive Care Unit, where, because of the decrease of the hemoglobin level, a blood transfusion with 4 units of red cells was carried out. In consideration of these findings prompted surgical consultation took place and the patients was transferred to our Surgical unit. Repeated CT scanning revealed 4 lesions ranging from 2-3 cm in the right hepatic lobe without signs of active bleeding and a diagnosis of adenomas or atypical multiple hemangiomas was made. The pa-tient was discharged from hospital 8 days later with no abnormality in hematological parameters and the liver function tests in the normal range. A Magnetic Resonance Imaging (MRI) (Figure 2) was performed in order to monitor the hepatic lesion and showed a significant reduction of subcapsular hematoma and confirmed the multiple lesions described above and confined to the right liver lobe. A right emihepatec-

tomy procedure was planned for resection of liver lesions. In February 2011 surgical exploration re-vealed two diaphragmatic nodules less than 1 cm in diameter that were excised, and a fresh-frozen sec-tion histology was made. Histologic examination re-vealed endometrial glands and stroma within hepatic tissue, suggesting the presence of an endometriosis cyst. A thorough exploration of the abdominal cavity revealed no evidence of other endometrial implants. Hepatic ultrasound was performed and showed a non-homogeneous mass in the V-VIII segments of 5 X 4 cm in the context of a steatotic parenchyma. The patient was submitted to right emihepatectomy using Cavitron Ultrasonic Aspirator (CUSA System 200, Val-leylab, Boulder, CO, USA). A permanent histological examination of hepatic parenchyma was consistent with metahemorrhagic endometriosis cysts (Figure 3) as well the diaphragmatic nodules. Immunohis-tochemical characterization was made on selected samples with a marker for endometrial glands, and the cytoplasm of stromal cells were strongly positive

Figure 1: Computed Tomography (CT) Scan of the Abdomen and Pelvis, Showing an Hyperdense Area with Small Arterial Blushes in the VI Segment and a Disomogeneous Lesion, with a Hypodense Margin, in the V Segment



Figure 2: Magnetic Resonance (MR) of the Abdomen and Pelvis, Showing a Significant Reduction of Subcapsular Hematoma and Confirming the Multiple Lesions Described above and Confined to the Right Liver Lobe

Figure 3: Peri-Hepatic Haemorragic Cyst



for Cluster of Differentiation (CD) 10 (Figure 4). Post-operative course was complicated by pulmonary embolism (although lower extremity echo-doppler showed no abnormality), treated with low-molecular-weight heparins and anticoagulant therapy thereafter up to 6 months. She was discharged ten days after surgery. One year after surgery the patient is asymp-tomatic. Surveillance Contrast Enhancement Ultra-sound (CEUS) demonstrated persisting multiple liver lesions (maximum diameter 2 cm) in the remnant he-patic left lobe. Transvaginal ultrasound demonstrated uterine endometriotic cysts. Hormone replacement therapy was contraindicated because of the high risk of thromboembolism; therefore, the patient has been treated with Gonadotropin-Releasing Hormone (GnRH) agonists.

DiscussionEndometriosis is an estrogen-dependent disorder that can result in substantial morbidity, including pelvic pain, multiple operations, and infertility which affects 6-10% of women in their reproductive years and af-fects up to 35-50% of women with pain or infertility [5].

Extra pelvic sites of endometriosis have been de-scribed varying from abdominal to thoracic organs. The only organ in the abdominal cavity that is appar-ently refractory to the disease is the spleen [7]. Hepat-ic endometriosis is an unusual phenomenon and sev-eral theories have been invoked to account for hepatic endometriosis, but the pathogenesis, especially in such rare cases, remains uncertain. The most widely accepted theory is based upon possible mechanisms

Figure 4: Peri-Hepatic Tissue with Hemorrhage, Hemosiderin Deposition, Macrophages and Endometrial-like Glands Surrounded by Spindled Endometrial Stroma (A, B, C) Strongly Positive for CD10 (D)



which transport endometrial tissue to distant sites in fashion analogous to metastatic spread of neoplasm. The proposed theories of endometrioma formation are retrograde spread of endometrial cell collections during menstruation, blood, lymphatic or iatrogenic spread, celomatic metaplasia of the pelvic peritoneal cell, immune system dysfunction and autoantibody formation [9, 10].

It is likely that a combination of these theories may apply to each individual patient. Two phenotypic situ-ations should be distinguished: 1) patients in whom the only endometriotic lesion is an intraparenchymal hepatic endometrioma; and 2) patients in whom the in-traparenchymal liver endometrioma is associated with endometriosis elsewhere. Some Authors postulated that the theory of embryonic mullerian rests [13] of-fered the best explanation for the pathogenesis of iso-lated hepatic endometriomas as well as the absence of endometriosis in the spleen [14], that presents an environment hostile to survival of embryonic mullerian rest. Organogenesis of the liver, spleen and muller-ian ducts begins in that order between the 2nd and 6th month of fetal life, affording an opportunity for duplicat-ed mullerian tissue to become incorporated in the liver and the spleen [12]. However, since the liver initially is the primary organ of hematopoiesis, the optimal conditions for vasculogenesis not only ensure survival of intrahepatic mullerian rest but also maintenance of full functional potential during the long interval of hormonal deprivation between withdrawal of placen-tal hormones and onset of estrogen stimulation [12]. With regard to the second phenotypic presentation as intraparenchymal hepatic endometrioma associated with endometriosis elsewhere, the theory of embry-onic mullerian rests probably still holds because there is no direct communication between uterine and liver lymphatics. Furthermore, vascular spread also could provide a plausible explanation for the pathogenesis of the intraparenchymal endometriosis in the liver [42].

The diagnosis of extrapelvic endometriosis may be challenging. Case reports described in literature dem-onstrated that medical history regarding pain may not be helpful in diagnosing hepatic endometriosis. This is also valid in our case where the upper abdominal pain associated with a bleeding lesion of the liver could be related to liver masses along with hepatocellular car-cinoma and adenoma both of which occur more com-monly. Since the lesion was bleeding, a percutaneous

liver biopsy was not performed. Although ultrasound, CT scan and MRI aid in the diagnosis, the final diag-nosis can be made only by pathologic evaluation, be-cause there are no radiological characteristics specific for the hepatic endometrioma. This is further compli-cated by the potentially fluctuating appearance of en-dometrial tissue under hormonal stimulation [6].

The laparoscopic approach may be recommended as an option for the diagnosis and the treatment of hepatic endometriosis in proper settings. One of the significant advantages of this minimally invasive pro-cedures is the thorough exploration of the abdominal cavity and pelvis, that could reveal endometriotic im-plants [14]. Frozen section histology at the time of sur-gery may help to avoid radical liver resection with no conversion to open surgery, when the size and the site of lesions could allow it [6].

In this context, it seems that no clues to hepatic endo-metriosis diagnosis can be gained from the history or examination and the imaging studies are not specific to this condition. For these reasons, early diagnosis may require a high degree of suspicion in women with liver mass.

In view of the present case report and the few ones described in the literature it is difficult to recommend a management strategy for this group of patients. In subjects with superficial lesions who are asympto-matic and are not treated, one should consider the possibility that these lesions may become infiltrative and symptomatic. When the patient is symptomatic, the need for treatment is clear. However, it remains undetermined whether asymptomatic patients should be treated to prevent the potentially severe and de-bilitating complications that can occur if the endometri-otic lesions deeply infiltrate the liver. Although rare, malignancy occurring within endometric foci has been well documented [25].

Hepatic endometriosis is a rare disorder character-ized by the presence of ectopic endometrium in the liver and its etiology and pathogenesis are unclear. The present case and the evidence in literature sug-gest that hepatic endometrioma should be included in the differential diagnosis for a woman of any age pre-senting with hepatic cystic or solid lesions of unknown cause, with or without a history of pelvic endometrio-sis. The lack of a clinical-radiological pattern makes it difficult to have a correct preoperative diagnosis, so



that it is made by histological examination. Surgery plays an important role in the treatment of HE, is re-lated to the symptoms and the potential for malignant transformation of the lesion as well [32].

ConclusionOur paper underlines that hepatic endometriosis may represent a diagnostic dilemma. In fact, considering that liver involvement in patients suffering from this disease is a rare event, its presentation may be unu-sual and imaging techniques may be inconclusive, be-cause of lack of a specific radiological pattern. To date, only a limited number of cases have been described in literature. In our clinical practice, we observed a 36 years old white Caucasian woman with hepatic endometriosis. The diagnosis required the combined assessment of different elements: clinical history, im-aging techniques, surgical exploration and histological examination. Therefore, we performed a systematic review of literature to evaluate the impact of this dis-orders in clinical practice. This case report highlights that physicians should consider this pathological con-dition, even if infrequent, in the differential diagnosis for a woman of any age presenting with hepatic cystic or solid lesions of unknown cause (with or without a history of pelvic endometriosis). A correct preopera-tive diagnosis is very difficult, and the recognition of this condition mainly relies on a proper assessment of anamnestic, radiological and histological data.

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Citation: Laura Mastrangelo, Michele Masetti, Maria Grazia De Blasiis, Paolo Emilio Orlandi, Angela Salerno, Dario de Biase, Sirio Fiorino and Elio Jovine, ”Hepatic Endometriosis: Systematic Review of Literature ANS A Case Report”, Global Scientific Research Journal of Surgery, 1(1), 2018, pp. 1-13.

Copyright © 2018 Laura Mastrangelo et al., This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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