Article:Endometriosis-associated clear cell carcinoma arising in caesarean section scar: a case report and review of the literature. (5135835)

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This page is the ScienceSource HTML version of the scholarly article described at https://www.wikidata.org/wiki/Q39027342. Its title is Endometriosis-associated clear cell carcinoma arising in caesarean section scar: a case report and review of the literature. and the publication date was 2016-12-03. The initial author is Gabriella Ferrandina.

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Converted JATS paper:

Journal Information

Title: World Journal of Surgical Oncology

Endometriosis-associated clear cell carcinoma arising in caesarean section scar: a case report and review of the literature

  • Gabriella Ferrandina
  • Eleonora Palluzzi
  • Francesco Fanfani
  • Stefano Gentileschi
  • Anna Lia Valentini
  • Maria Vittoria Mattoli
  • Ilaria Pennacchia
  • Giovanni Scambia
  • Gianfranco Zannoni

Publication date (epub): 12/2016

Publication date (pmc-release): 12/2016

Publication date (collection): /2016

Abstract

Background

Malignant transformation has been reported in approximately 1% of the endometriosis cases; herein, we report a case of clear cell endometrial carcinoma arising from endometriosis foci located within a caesarean section scar.

Case presentation

In November 2014, a Caucasian, 44-year-old woman was transferred to our institution because of severe respiratory failure due to massive lung embolism and rapid enlargement of a subcutaneous suprapubic mass. Abdomino-pelvic magnetic resonance showed a 10.5 × 5.0 × 5.0 cm subcutaneous solid mass involving the rectus abdominis muscle. Pelvic organs appeared normal, while right external iliac lymph nodes appeared enlarged (maximum diameter = 16 mm). A whole-body positron emission tomography/computed tomography scan showed irregular uptake of the radiotracer in the 22 cm mass of the abdominal wall, and in enlarged external iliac and inguinal lymph nodes. In December 2014, the patient underwent exploratory laparoscopy showing normal adnexae and pelvic organs; peritoneal as well as cervical, endometrial and vesical biopsies were negative. The patient was administered neo-adjuvant chemotherapy with carboplatin and paclitaxel, weekly, without benefit and then underwent wide resection of the abdominal mass, partial removal of rectus abdominis muscle and fascia, radical hysterectomy, bilateral salpingo-oophorectomy, and inguinal and pelvic lymphadenectomy. The muscular gap was repaired employing a gore-tex mesh while the external covering was made by a pedicled perforator fasciocutaneous anterolateral thigh flap. Final diagnosis was clear cell endometrial adenocarcinoma arising from endometriosis foci within the caesarean section scar. Pelvic and inguinal lymph nodes were metastatic. Tumor cells were positive for CK7 EMA, CKAE1/AE3, CD15, CA-125, while immunoreaction for Calretinin, WT1, estrogen, and progesterone receptors, cytokeratin 20, CD10, alpha fetoprotein, CDX2, TTF1, and thyroglobulin were all negative. Liver relapse occurred after 2 months; despite 3 cycles of pegylated liposomal doxorubicin (20 mg/m2, biweekly administration), the death of the patient disease occurred 1 month later.

Conclusions

Attention should be focused on careful evaluation of patient history in terms of pelvic surgery, and symptoms suggestive of endometriosis such as repeated occurrence of endometriosis nodules at CS scar, or cyclic pain, or volume changes of the nodules.

Paper

Background

Malignant transformation has been reported in approximately 1% of the endometriosis cases, and most frequently this transformation takes place at the ovary, accounting for about 80% of the endometriosis-associated malignancies [[1]].

Endometriosis occurring in surgical abdominal scar has been mainly documented after caesarean section (CS) or hysterectomy (0.03 up to 0.4%), and its malignant transformation is very rare [[2]]: clear cell histology accounts for only 4.5% of extragonadal endometriosis-associated malignancies, while representing the most common histotype in case of parietal localization [[1]].

Given the rarity of malignant transformation of abdominal scar endometriosis to clear cell histology, pathogenesis and risk factors of this disease are hardly assessable [[3]]. Nonetheless, due to the increased rate of CS registered in the last years, we can expect a parallel increase of endometriosis implants in the CS scar and occurrence of clear cell carcinoma (CCC) of the abdominal wall.

Herein, we report a new case of CCC arising from endometriosis foci located within a CS scar; a systematic review of the available literature relative to this issue is also presented.

Case presentation

In November 2014, a Caucasian, 44-year-old woman was transferred to our institution from the emergency unit of another hospital where she had been successfully treated for a severe respiratory failure due to massive lung embolism and cardiogenic shock.

Her familial history was uneventful; she had undergone one caesarean section 9 years before without complications and had assumed oral contraceptives until the appearance of symptoms. She had never suffered from signs or symptoms of endometriosis.

The patient referred to have documented, since the last 5 months, the slow enlargement of a suprapubic mass at the CS scar (lower abdominal incision) and abdominal swelling.

In July 2014, she had already performed abdomino-pelvic magnetic resonance imaging (MRI) showing a 10.5×5.0×5.0 cm subcutaneous solid mass with cystic areas and internal septa involving the rectus abdominis muscle. The mass appeared strictly adherent to the uterus and recto-sigma. Pelvic organs appeared normal, while right external iliac lymph nodes appeared enlarged (short axis maximum diameter = 16 mm).

The patient had been already triaged to fine needle aspiration (FNA) of the mass which was suggestive of endometrial tubule-papillary carcinoma.

At physical examination, a suprapubic mass of almost 20 cm maximum diameter was documented close to the midpoint of the CS scar (Fig. 1a–c). Laboratory tests revealed normal levels of CEA, CA125, and squamous cell carcinoma antigen.Fig. 1

Clinical appearance of the patient at time of presentation (ac): a large mass (a, b) extended from the pubic symphysis to the umbilicus was evident; the mass appeared mainly solid with some cystic lesions on the surface. The caesarean section scar is evident (white arrow). Appearance of the abdominal reconstruction after 2 months from surgery (d)

Once the patient recovered from the acute phase of lung embolism and achieved haemodynamic compensation, a whole-body positron emission tomography/computed tomography (PET/CT) scan was performed about 60 min after the intravenous administration of 18F-FDG (148 MBq), showing irregular/non-homogeneous uptake of the radiotracer in the 22 cm mass of the abdominal wall. Increased 18F-FDG uptake was also seen in enlarged external iliac and inguinal lymph nodes bilaterally (Fig. 2b, c, e, f). Abdomino-pelvic MRI performed in our institution documented normal uterus and adnexae, and confirmed the presence of the anterior abdominal wall mass composed of solid as well as locular areas; the mass completely infiltrated the rectus muscle of abdomen and extended up to the skin surface, while displacing intestinal loops. The cleavage planes neighboring the uterus and bladder appeared preserved as well as the inguinal, external iliac, and obturator lymph nodes (Fig. 2a, d).Fig. 2

Pre-surgical T2-weighted FSE sagittal MRI (a) documenting a supra-vesical pelvic mass extending into the anterior pelvic wall and showing non-homogeneous signal intensity and solid components. Sagittal CT (b) and fused 18F-FDG PET/CT (c) images showed non-homogeneous uptake in the 22 cm abdominal mass: in particular, intense abnormal 18F-FDG uptake was present in the caudal solid component of the mass, whereas an absent area of tracer uptake was evident in its cranial fluid component. Corresponding T2-weighted FSE axial MRI (d) confirmed the presence of a solid and partially fluid pelvic mass, and enlarged loco-regional lymph nodes (arrow). Axial CT (e) and fused 18F-FDG PET/CT images (f) showed intense tracer uptake in the solid component of the mass, extended up to the skin surface of pelvis, and enlarged left external iliac lymph-node, characterized by increased tracer uptake (arrows)

In December 2014, the patient underwent exploratory laparoscopy showing normal adnexae and pelvic organs; peritoneal as well as cervical, endometrial, and vesical biopsies were negative.

Considering the results of FNA suggesting primary Müllerian-derived carcinoma and the extent of disease whose radical resection would require widely demolitive surgical procedures, the patient was triaged to neo-adjuvant chemotherapy with carboplatin (AUC = 2), and paclitaxel (80 mg/m2), every week. After 3 cycles (9 administrations) MRI documented only a slight reduction of the mass and lymphadenopathies, thus leading to consider the need of a multidisciplinary approach with gynecologic and medical oncologists, surgeons, and plastic surgeons in order to plan the most adequate patient treatment. After a thorough evaluation, radical surgery with reconstruction was planned, and an extensive counseling was carried out with the patient and her relatives.

At the beginning of March 2015, the patient underwent wide resection of the abdominal mass, partial removal of rectus abdominis muscle and fascia; moreover, radical hysterectomy, bilateral salpingo-oophorectomy (BSO) as well as inguinal and pelvic lymphadenectomy were performed.

At the end of surgery, the abdominal wall defect appeared as a round hole of 14 × 14 cm which involved the abdominal wall thickness completely. The muscular gap was repaired employing a gore-tex mesh anchored directly on the residual rectus muscles and sheets. The external covering had been planned by a pedicled perforator fasciocutaneous anterolateral thigh flap. The perforator vessels from the descending branch of the lateral circumflex femoral artery had been preoperatively located, with ultrasound doppler sonography, at the level of the intermuscular lateral septum of the thigh. The right thigh was chosen as donor site because the perforators were more distal, thus allowing to lengthen the pedicle. The donor site, on the right thigh, was repaired both by direct closure, and a skin graft harvested from the contralateral thigh. Postoperative course of the wounds was uneventful and stitches were removed at 2 weeks. The patient was discharged after 18 days in good clinical conditions, and the cosmetic result was acceptable (Fig. 1d).

Macroscopically, the surgical specimen consisted of cutis and subcutaneous tissue which contained a capsulated tumor mass measuring 18 cm in maximum diameter, infiltrating the rectus abdominis muscle. The cut surface was whitish and showed areas of necrosis and hemorrhage. Histological examination of tissue samples revealed neoplastic proliferation of large-sized, epitheliomorphous cells with abundant clear or occasionally eosinophilic cytoplasm and prominent nucleoli. A remarkable degree of nuclear atypia with diffuse hyperchromasia and irregular nuclear contours, and cellular pleomorphism was evident throughout the whole lesion. Architecturally, the tumor featured a mixed pattern of growth, both solid and tubulocystic, occasionally including distinctive papillary areas with hyalinized stromal cores. The clear cells lining the papillae and the cystic spaces showed the characteristic hobnail appearance. A few eosinophilic hyaline globules were observed as well (Fig. 3a–c). Interestingly, sparse foci of endometriosis were present in the fibrous adipose tissue all around. Surgical margins were free of disease.Fig. 3

The tumor displayed a mixed pattern of both tubulocystic and papillary growth, HE x5 (a), and HEx10 (b); cells were large with abundant clear or occasionally eosinophilic cytoplasm. Note the high-grade nuclear atypia, HEx20 (c); neoplastic cells showed positive cell membrane immunostaining for CK7 (x20) (d)

Immunohistochemical investigation showed positive tumor cell reaction for CK7 (Fig. 3d), EMA, CKAE1/AE3, CD15, CA-125. On the contrary, immunoreaction for Calretinin, WT1, estrogen, and progesterone receptors, cytokeratin 20, CD10, alpha fetoprotein, CDX2, TTF1, and thyroglobulin were all negative. Hence, the morphologic findings and the immunohistochemical results were consistent with a diagnosis of clear cell adenocarcinoma most likely arising in the setting of an abdominal wall endometriosis. Lymph node involvement was documented in 7 out of 14 pelvic lymph nodes, and in 8 out of 11 inguinal lymph nodes.

After 2 months from surgery, the patient was submitted to total body CT scan in order to plan subsequent adjuvant treatment. Despite the absence of disease in the pelvis, CT scan documented the appearance of six neoplastic lesions (from 2.7 to 5.5 cm maximum diameter) in the liver. Treatment with pegylated liposomal doxorubicin (20 mg/m2, biweekly administration) was started, and CT scan evaluation after 3 cycles showed the progression of hepatic involvement and appearance of ascites. The death of the patient disease occurred 1 month later.

Discussion

We have provided an additional patient to the series of 22 cases of endometriosis-associated CCC arising within CS scar, as reported in the literature [[4][24]]. Only 2 reports were not available from the requested authors.

Despite the rarity of this condition, the number of reported cases has increased over time (see Table 1) likely due to a higher attention focused on this disease, but also to the increased rate of CS and uterine surgeries documented over time. Therefore, more diffuse awareness of this condition and better understanding of its pathogenesis could be important to provide early diagnosis and more effective treatment.Table 1

Clear cell carcinoma arising from endometriosis of the scar caesarean section

Age Previous uterine surgeries Months since symptoms Size cm FNA or biopsy Primary treatment Pathology Adjuvant treatment Relapse Death
Schnieber Agner-Kolb 1986 [[4]] 40 1 CS 15 years before WE, BSO, Hys Mass: CCC + endometriosisOvaries and uterus: negative RT, progestins Yes after 18 months
Hitti, 1996 [[5]] 46 1 CS 14 years before1 CS 12 years before 6 WE, BSO, Hys CCC + endometriosis RT No after 30 months No after 30 months
Miller 1998 [[6]] 38 1 hysterotomy 9 years before1 abortion 3 years before1 CS 2 years before 8 4 CCC + endometriosis WE, BSO, Hys omentectomy Scar: CCCOvaries, uterus, omentum: negativeMargins: close CIS-based CTRT No after 60 monthsd No after 60 monthsd
Park 1999 [[7]] 56 1 CS 24 years1 CS 20 years 5 WE Mass: CCC + endometriosis RT
Ishida 2003 [[8]] 56 1 CS 24 years1 CS 20 years 7 10 Endometrial carcinoma WE, Hys, BSO Mass: CCCOvaries and uterus: negative CIS-based CT Yes after 24 monthsb
Sergent 2006 [[9]] 45 1 CS 25 years1 CS 23 years2 excisions of benign endometriosis nodules at the scar 17 20 WE, BSO,later on: endometrial curettage Mass: CCC + endometriosisRight ovary: benign endometriosis; left ovary and uterus: negativeMargins: 1 cm free Not done Yes early after surgerya Yes after 6 months
Alberto 2006 [[10]] 38 1 CS 11 yearsBSO, Hys for endometriosis 6 6 WE CCC Carbo/PTXRT
Razzouk 2007 [[11]] 46 1 CS 26 years before1 CS 24 years before2 excisions of endometriosis nodules at the scar >20 GnRh analogue without benefit WE, BSO Mass: CCC + endometriosisOvaries: negativeLN: 1 positive Carbo/PTX Yes during CT Yes after 6 monthsb
Rust 2008 [[12]] 42 3 CSHys 5 years before 24 5 Carcinoma WE Mass: CCC + endometriosisMargins: 1 mm free Not done
Bats 2008 [[13]] 38 1 CS 13 years before1 excision of endometriosic nodule at the scar 10 Atypical cells NACT (carbo/PTX)No benefit WE, BSO, Hys, omentectomy Mass: CCC + endometriosisUterus: adenomyosisOther specimens: negativeMargins: 2 mm free Not done Yes after 4 monthsa
Williams 2009 [[14]] 53 1 CS 17 years before 24 2.5 CCC (excisional biopsy) WE of the scar, BSO, Hys, omentectomyInguinal/Pelvic LNctomy Mass: CCCUterus, right ovary, omentum: negative, left ovary: teratomaInguinal LN: 7 positive/11Pelvic LN: 8 positive/14 Carbo/PTX (4 cycles) Yes after 3 monthsa Yes after 11 monthsb
Bourdel 2010 [[15]] 43 1 CS 20 years before1 CS 15 years before1 excision of endometriosic nodule at the scar 9 9 WE, partial resection of pubic symphysis, umbilicus, right rectus abdomen, pelvic LN samplingLater on: BSO, Hys Mass: CCC + endometriosisPelvic LN: multiple positiveOvaries, uterus: negative Carbo/PTX (6 cycles)RT Yes after 6 monthsd Yes after 22 monthsb
Yan 2011 [[16]] 41 2 CS 5 years before2 excisions of benign endometriosic nodule at the scar 1 year and 4 months before 4 9 Not done Progestins without benefit WE Mass: CCC CT No after 24 monthsd No after 24 monthsd
Li 2012 [[17]] 49 1 CS 26 years before 25 years 9 Not done WE, Hys, BSO Mass: CCCUterus, ovaries: negative Carbo/PTX (6 cycles) Noc after 8 months Noc after 8 months
Mert 2012 [[19]] 42 Tubal ligation, right ovariectomy 15 Tumor cells Mullerian origin NACT (carbo/PTX) WE, left SO Hys, left Pelvic LNctomy Omentectomy Mass: CCC + endometriosisOther organs: negativeMargins: free Not done No after 1 montha No After 1 montha
51 2 CS Hys for myomas 12 6 Excisional biopsy CCC + endometriosis BSO, Omental biopsy NegativeMargins: free RT No after 31 monthsb No after 31 monthsb
Shalin 2012 [[18]] 47 1 CS 10 3 CCC WE, left ovary cystectomy, endometrial biopsy, pelvic LN sampling Mass: CCC + endometriosisOvarian cyst: endometriosisEndometrium: negativePelvic LN: 2 positive/4Margins: positive CIS-based CT (6 cycles)RT Yes after 5 monthsb No after 7 monthsb
Ijichi 2014 [[20]] 60 1 CS 37 years before1 CS 35 years before 48 4 Atypical cells WE Mass: CCC + endometriosisMargins: free Not done Yes after 8 monthsa No after 23 monthsa
Aust 2015 [[21]] 47 1 CS 16 years beforevaginal Hys 10 yearsbefore 6 10 WE Later on: BSO, pelvic, aortic LNctomy omentectomy Mass: CCCOvaries and omentum: negativeLN:2 positive/48Margins: free Carbo/PTX (6 cycles) No after 10 monthsc No after 10 monthsc
Heller 2014 [[22]] 37 1 CS1 CS1 CS 8 years before 96* 18 CCC WE, left SO, pelvic LNctomy Mass: CCCOvary: negativeLFN: multiple LN positive Refused treatment Yes after 5 monthsa
Liu 2014 [[23]] 39 1 CS1 excision of endometriosic nodule at the scar 60 6 WE, partial cystectomy, BSO, Hys, omentectomy, inguinal,pelvic, aortic LNctomy Mass: CCC + endometriosisOvaries, uterus, omentum: negativeBladder: positivePelvic LN: 18 positive/21Aortic LN: 6 positive /6Inguinal LN: 8 positive/8 Carbo/PTX (3 cycles) YES after 10 monthsc Yes after 12 monthsc
Sosa-Duràn 2015 [[24]] 45 1 CS1 CS1 CS 6 9 WE, margins: 2 cm free Mass: CCC + endometriosis Not done No after 16 monthsa No after 16 monthsa
Current case 44 1 CS 9 years before 8 22 Endometrial carcinoma NACT (carbo/PTX)WE, BSO, Hys, inguinal, and pelvic LNctomy Mass: CCC + endometriosisOvaries, uterus: negativePelvic LN: 7 positive/14Inguinal LN: 8 positive/11Margins: free Not done Yes after 2 months from surgery Yes after 6 months

CCC clear cell carcinoma, CS caesarean section, WE wide mass excision, BSO bilateral salpingo-oophorectomy, SO salpingo-oophorectomy, Hys hysterectomy, LNctomy lymphadenectomy, LN lymph node, Carbo carboplatin, CIS cisplatin, PTX paclitaxel, RT radiotherapy

*The mass was reported to have come and gone over the last 8 years since the last CS

aFrom surgical resection

bFrom initial diagnosis

cSince completion of chemotherapy

dNot specified

Even though the criteria for the diagnosis of endometriosis-associated malignancies include also the coexistence of neoplastic endometrial tissue and endometriosis, almost one third of CCC arising within CS scars were not associated with endometriosis foci (Table 1). However, it has to be considered that four patients had referred cyclic pain in the CS scar during menses, or the cyclic increase/decrease of the mass volume, which could be highly suggestive of the presence of endometriosis implants [[14], [17], [19], [23]]. Moreover, previous history of the excision of benign endometriosis foci at the CS scar was reported in five cases [[9], [11], [13], [15], [16]]. Therefore, the absence of pathologically assessed endometriosis foci could be interpreted as either a sampling problem or a consequence of the complete replacement of normal tissue due to massive neoplastic proliferation. In this context, careful collection and evaluation of patient history would be important to have a high index of suspicion for endometriosis-associated malignancy.

Indeed, these masses usually reach very large dimensions (median diameter: 9 cm, range 2.5 up to 22 cm) (Table 1) before the diagnosis is made, thus highlighting the difficulties to suspect this condition and obtain an early diagnosis. This is clinically relevant since primary surgical treatment very frequently requires wide surgical excision of the mass together with partial removal of part of the abdominal muscles and reconstructive surgeries with a mesh or even pedicle-skin-muscle flap. Demolitive surgery was also necessary in the 3 cases initially triaged to neo-adjuvant chemotherapy ([[13], [18]] current case), since only 1 of them achieved partial response after 8 cycles of carboplatin/paclitaxel chemotherapy [[18]]; in addition, wide excision was necessary in the 2 cases who had undergone excision of endometriosis nodules at the CS scar in the past, and had been unsuccessfully treated with GnRh and progestins, respectively, before being triaged to radical surgery which led to definitive diagnosis of malignancy. Besides wide resection of the mass, other surgical procedures were often carried out including BSO (82.6%), as well as hysterectomy (71.4%), or endometrial biopsy (9.5%, and omentectomy or omental biopsy (30.4%), in order to exclude other primary tumors sites.

Despite the aggressiveness of surgery and the multimodal treatment approach, of 18 cases with available follow up data, 10 experienced relapse of disease, mostly at distant sites, and 8 patients died of disease.

Apart from the long time interval to diagnosis and the wide extension of disease in the abdominal wall, clinical aggressiveness is also sustained by the intrinsic biologic aggressiveness of CCC, which differs from other endometrial cancer histotypes. In this context, proper diagnosis should take advantage of immunohistochemical panels with several markers in order to exclude serous histotype as well as mesothelial tumors such as malignant mesothelioma and papillary mesothelioma which are usually positive for Calretinin, WT1, and keratin 5/6, contrary to what is observed in CCC. In addition, WT1 is the most important immunohistochemical marker to distinguish serous carcinoma from CCC.

It has to be acknowledged that of 9 cases undergoing lymphadenectomy or sampling, 8 showed diffuse metastatic involvement of inguinal, and/or pelvic, and/or aortic lymph nodes ([[11], [14], [15], [19], [22], [23]] current case).

On the other hand, some cases were reported to experience relatively longer disease-free and overall survival (≥30 months) [[5], [6], [16], [18]]; while recognizing that a more thorough molecular characterization could hopefully help define prognosis of this very rare condition, it has to be acknowledged that cases with better outcome presented with masses ranging between 4 and 9 cm, thus suggesting that a prompt recognition and treatment could make the difference.

Obviously, also prevention of endometriosis implantation at time of CS is of utmost importance: as recently emphasized, the uterus should not be exteriorized, exposure of endometrial mucosa during uterus suturing should be limited, and peritonization may be advised, although there is no definitive data about these issues [[15]].

Conclusions

Attention should be focused on careful evaluation of patient history in terms of pelvic surgery, and symptoms suggestive of endometriosis such as repeated occurrence of endometriosis nodules at CS scar, or cyclic pain, or volume changes of the nodules.

Acknowledgements

Acknowledgements

None.

Funding

No funding source to be declared.

Availability of data and materials

All data (imaging, pathology, immunohistochemistry, and procedures) are available.

Authors’ contributions

GF participated in the management of the patient and wrote the case report. EP participated in the medical management of the patient. FF was involved in the surgical management of the patient. SG carried out plastic surgery. ALV contributed to imaging characterization. MVM carried out imaging characterization. IP performed immunohistochemistry and contributed to pathological characterization. GS participated in the management of the patient and contributed to manuscript writing. GZ was in charge of immunohistochemistry and pathological diagnosis. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

We have obtained consent to publish from the legal relative (husband) of the patient, since she passed away before the manuscript planning and writing.

According to our institutional ethical committee, no specific protocol is required for retrospective collection of data.

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The underlying source XML for this text is taken from https://www.ebi.ac.uk/europepmc/webservices/rest/PMC5135835/fullTextXML. The license for the article is Creative Commons Attribution 4.0 International. The main subject has been identified as endometrial carcinoma.