
==== Front
Int J Surg Case Rep
Int J Surg Case Rep
International Journal of Surgery Case Reports
2210-2612
Elsevier

S2210-2612(24)01016-2
10.1016/j.ijscr.2024.110235
110235
Case Report
Concurrent rectosigmoid cancer and Krukenberg tumor in a pregnant patient: A rare clinicopathological presentation - Case report
Benali Saad a1
Benlghazi Abdelhamid benlghaziabdelhamid333@gmail.com
a1⁎
Messaoudi Hamza a
El Agouri Hajar b
Belouad Moad a
Kouach Jaouad a
a Department of Gynecology-Obstetrics, Mohammed V Military Teaching Hospital, Faculty of Medicine and Pharmacy of Rabat, University Mohammed V, Rabat, Morocco
b Department of Pathology Mohammed V Military Teaching Hospital, Faculty of Medicine and Pharmacy of Rabat, University Mohammed V, Rabat, Morocco
⁎ Corresponding author at: Department of Gynecology and Obstetrics Military Hospital Mohammed V Rabat, Faculty of Medicine and Pharmacy of Rabat, University Mohammed V Rabat, Morocco. benlghaziabdelhamid333@gmail.com
1 The first 2 authors contributed equally to the development of this document.

03 9 2024
10 2024
03 9 2024
123 1102352 8 2024
26 8 2024
31 8 2024
© 2024 The Authors. Published by Elsevier Ltd on behalf of IJS Publishing Group Limited.
2024

https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction and importance

The occurrence of ovarian tumors during pregnancy is relatively low, with an incidence of approximately 0.05 %. Both primary ovarian cancer and metastatic malignancies are uncommon in pregnant women, and there is often a delay in diagnosing these conditions.

Case presentation

We report the case of rectal cancer with ovarian metastasis discovered in a 36-year-old multiparous pregnant woman who presented at 21 weeks gestation with constipation and increased abdominal volume over the past three weeks. These symptoms were associated with loss of appetite and general fatigue. Further investigations revealed a 12 × 9 cm mass on the left side of the uterus and a 5.2 × 4 × 3.6 cm mass in the recto-sigmoid region. Initially, the patient underwent left adnexectomy, peritoneal cytology, biopsies of the peritoneum, epiploic region, and right ovary. Subsequently, the pregnancy was continued until 34 weeks' amenorrhea, when the fetus was extracted, and a complete surgical procedure was performed, including total hysterectomy, right adnexectomy, resection of the recto-sigmoid tumor with appendectomy and infra-gastric omentectomy. After surgery, the patient received adjuvant chemotherapy.

Clinical discussion

It is important to consider the possibility of malignancy during pregnancy when atypical clinical presentations occur. Gastrointestinal cancer is the most common cause of Krukenberg's tumor in pregnant women. Early diagnosis of cancer at an operable stage is essential to improve prognosis.

Conclusions

This clinical case highlights the rarity of Krukenberg's tumor during pregnancy and the challenges encountered in diagnosing and treating this disease.

Highlights

• Krukenberg metastasis in pregnancy is a rare diagnosis.

• The main difficulty in diagnosis resides in the shared common symptoms.

• The diagnosis is confirmed by histopathology and immunohistochemistry.

• Multiple disciplinary collaboration is essential for effective outcomes.

Keywords

Case report
Rectosigmoid cancer
Pregnancy
Krukenberg
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pmc1 Introduction

Krukenberg tumors (KT) are rare tumors that account for 1 to 2 % of ovarian tumors. They were described in 1895 by Friedrich Krukenberg as metastatic ovarian localizations of a gastrointestinal adenocarcinoma. It usually involves bilateral ovarian involvement and the prognosis is poor. Few cases have been published concerning the association of KT and pregnancy (1). The low incidence of this association is correlated to the rarity of digestive tumors in young women. Diagnosis becomes very difficult during pregnancy, the clinical picture being highly polymorphic and therapeutic management being limited by the pregnancy context (2).

We report the case of a 36-year-old multiparous pregnant woman who presented at 21 weeks of pregnancy and was diagnosed with a Krukenburg tumor. This case was presented in accordance with the updated consensus Surgical Case Report (SCARE) guidelines (3).

2 Case report

This is a case report of a 36-year-old patient, G3P2, who had previously undergone cholecystectomy. There was no familial history of neoplasia. The patient's third pregnancy was estimated to be at 21 weeks of amenorrhea and 2 days, and it proceeded without any significant complications.

The disease history began 20 days before admission, at 18 weeks of amenorrhea. The patient experienced gradually worsening constipation accompanied by an increase in abdominal volume. However, there were no reports of vomiting or rectal bleeding. These symptoms were observed in the context of fatigue and absence of fever. Upon clinical examination, the patient was found to be in relatively good overall condition, with a blood pressure reading of 120/75 mmHg. No uterine contractions were detected.

During the abdominal examination, it was observed that the abdomen was distended, and there was a sloping dullness on the flanks. No collateral venous circulation or palpable mass was detected. Gynecological and obstetrical examination did not reveal any notable findings.

Initially, the patient underwent an abdominopelvic ultrasound, which revealed a gravid uterus with an ongoing pregnancy, consistent with the estimated gestational age. The amniotic fluid was within the normal range, and the placenta was previa. A left lateral-uterine mass measuring 12 × 9 cm was visualized. The mass exhibited both solid and cystic components, displaying heterogeneous appearance with vegetations within the cyst and a thickened wall. Based on these findings, it was classified as ORADS 5, raising suspicion of malignancy. The right ovary appeared normal on the ultrasound. Additionally, a small amount of free fluid was noted.

Subsequently, a pelvic MRI was performed (Fig. 1) revealing a uterus carrying an ongoing pregnancy with a placenta located posteriorly and a left lateral-uterine ovarian mass measuring 130 × 90 mm. The mass is oval, well delineated with regular contours, and has a solid cystic component with a fleshy portion showing an isointense T2 signal. An exophytic tumor measuring 52 × 40 × 36 mm was present in the recto-sigmoid region. It showed central necrosis on the right wall, extending to mesorectal adipose tissue and fascia. The lesion was heterogeneous, predominantly isointense to soft tissue in the various imaging sequences, with areas hypointense in T1, hyperintense in T2, and irregular contours. A moderate-volume peritoneal effusion was also noted accompanied by several peritoneal nodules and nodular thickening of the greater omentum. The right ovary showed no abnormalities, and no lumbo-aortic or pelvic lymphadenopathy was visible. The CA 125 level was elevated, reaching 150 U/ml.Fig. 1 Pelvic MRI in T2 coronal, out-of-phase axial and T2 axial sections in a woman in her second trimester, showing a left latero-uterine mass Image 1 at the expense of the ovary, well-defined oval with regular contours, solid cystic with a fleshy portion in T2 isosignal. There is a copious peritoneal effusion. Note: pregnant uterus Image 2.

Fig. 1

An exploratory laparoscopy was indicated which revealed the presence of a highly suspicious left ovarian process with no lesion of peritoneal carcinosis or associated hepatic or digestive involvement. Given the possibility of total resection of the mass, the procedure was converted to a median laparotomy with peritoneal cytology, left adnexectomy, peritoneal and epiploic biopsies, and biopsies of the right ovary.

Histology was consistent with WHO grade 2 sero-mucinous carcinoma (Fig. 2).Fig. 2 (a): Tumor cells show diffuse positive labelling with anti-CDX2 antibody (IHC, G 200).

(b): Tumor proliferation with tubulopapillary architecture, pseudostratified and moderately atypical nuclei (HE stain, G 200).

(c): Tumor cells show positive labelling with anti-CK20 antibody (IHC, G 200).

Fig. 2

Peritoneal, right ovarian and epiploic biopsies and cytology were free of tumor cells. In the presence of the mass in the recto-sigmoid region, recto-sigmoidoscopy was performed, revealing an ulcerated low rectal tumor located 6 cm from the anal verge. A biopsy was performed and confirmed the presence of a moderately differentiated adenocarcinoma with myometrial invasion.

Following the multidisciplinary consultation meeting (oncologists, interventional radiologists, obstetricians, surgeons and pediatricians), a joint meeting was convened with the family to communicate the diagnosis and prognosis and present the available therapeutic options. The consensus decision was to proceed with fetal extraction via cesarean section at 34 weeks of gestation after achieving lung maturation through a course of betamethasone-based corticosteroid treatment. This would be followed by a comprehensive surgical procedure including total hysterectomy, right adnexectomy, resection of the recto-sigmoid tumor with appendectomy, and infra-gastric omentectomy. Cesarean section resulted in the birth of a male neonate with an Apgar score of 10/10. Birth weight was 2800 g and no significant malformations were observed.

Pathology confirmed the presence of a well-differentiated Leiberkühn's adenocarcinoma infiltrating the recto-sigmoid wall down to the sub-serosa, with the presence of mucus-filled catkin ring cells with excentric nuclei at PAS positives and the presence of vascular emboli and perineural sheathing.

The surgical margins were free of tumors. Involvement was also seen in the left horn and infra-gastric omentum. The parametrium, cervix, right tube, appendix, peritoneal cytology, and placenta were unremarkable.

The results of the thoracic-abdominal-pelvic CT scan did not indicate any additional secondary sites of metastasis. The tumor was classified as T3N0M1.

A total of 4 cycles of adjuvant chemotherapy were administered using the Folfox regimen (oxaliplatin, calcium folinate, 5-FU), followed by a switch to oral capecitabine for 2 cycles.

Unfortunately, a hepatic metastatic relapse was detected immediately after the completion of the 6th cycle of adjuvant chemotherapy. Histological proof of the liver lesion was not performed, given the patient's poor condition.

In response to this, the decision was made to initiate first-line palliative chemotherapy utilizing the FOLFIRI regimen (irinotecan, folinate, and 5-FU), in combination with targeted therapy using panitumumab, for a total of 6 cycles. Subsequently, a maintenance phase using 5-FU and folinate would be continued for an additional 6 cycles.

3 Discussion

Krukenberg's tumor is a metastatic adenocarcinoma of the ovary and accounts for 30–40 % of metastatic ovarian cancers. Gastro-intestinal cancer is the most common cause. Pregnancy-associated ovarian tumors are sporadic, with an incidence of 1 per 25,000 pregnancies (1). Studies indicate an increased risk of Krukenberg tumors in young women due to ovarian blood flow. Spread mechanisms include lymphatic, hematogenous, or trans-coelomic routes, involving dissemination through lymphatic channels, blood vessels, or adjacent organs. (4).

The main challenge in diagnosis lies in the similarity of the symptoms of pregnancy and the presence of colorectal cancer (CRC). Common symptoms of CRC include rectal bleeding, nausea, vomiting, constipation, and abdominal pain. During pregnancy, constipation and abdominal pain are common due to increased pressure from the uterus or slowed bowel movements. Rectal bleeding during pregnancy is often attributed to hemorrhoids or anal fissures (5). During pregnancy, weight is expected to increase, but it is not uncommon for some women to lose weight in the first trimester. However, weight loss is also a symptom of CRC, which may delay diagnosis in a pregnant patient or lead to diagnosis at a later stage of pregnancy (2).

In cases where pregnant women experience persistent gastrointestinal symptoms that do not improve with standard treatments, it is advisable to consider an endoscopic examination (2).

Ultrasound is a safe, rapid, and non-irradiating method of detecting Krukenberg metastases. These metastases may be solid (primary tumor of the stomach), mixed solid and cystic (primary tumor of the colon, rectum, appendix, or bile ducts), or, more rarely, predominantly cystic (primary tumor of the colon or appendix). Doppler analysis generally reveals scattered tumor vessels with little impeded blood flow (6).

On CT scan, the ovaries are replaced by bilateral solid, mixed solid, and cystic or predominantly cystic pelvic masses. The CT scan assesses extragenital extension and looks for a primary extra-ovarian tumor (7).

On MRI, the solid components of KT appear hypointense in T1 and T2 due to a dense stromal reaction, with diffusion restriction and enhancement after contrast injection. Cystic areas are T2 hyperintense due to mucin, which does not enhance. KT are characterized by hypointense T2 solid components, an oval configuration, clear margins, and intense enhancement after contrast injection, with a type 3 contrast uptake curve (7).

The diagnostic reliability of serum markers (CA 125, CA19–9, CEA) in digestive cancer is hindered by limited sensitivity and specificity, as well as inherent limitations related to pregnancy.

KT are diagnosed through histological evaluation based on established criteria by the World Health Organization. Criteria include poorly differentiated adenocarcinoma infiltrating ovarian stroma, mucin-producing neoplastic cells, and sarcomatoid tissue proliferation. Immunohistochemical staining helps determine tumor type, distinguishing between primary ovarian carcinoma and metastatic gastrointestinal carcinoma (8) (Table 1).Table 1 Comparison of common immunohistochemical profiles and tumor markers for different ovarian metastases versus primary ovarian tumors.

Table 1Malignancy type	CK7	CK20	CEA	CA-125	
Primary ovarian	+	−	−	+	
Gastric	−	+	+	−	
Colorectal	−	+	+	−	
Appendix	+	−	+	−	
Note—Plus sign (+) denotes present, and minus sign (−) denotes not present. CK7 = cytokeratin 7, CK20 = cytokeratin 20, CEA = carcinoembryonic antigen, CA-125 = cancer antigen 125.

The management of primary carcinoma of the rectum during pregnancy is tailored to each individual based on factors such as the stage of pregnancy, the stage and location of the tumor, and the presence of any complications. Currently, there is no universally accepted standardized treatment protocol for this particular situation (9).

The management of KT associated with pregnancy encompasses two aspects: pregnancy management and tumor treatment. Diagnosing adnexal masses during pregnancy is challenging, as distinguishing malignant ovarian neoplasms from benign conditions is difficult. Exploratory procedures (peritoneal biopsies and cytology, biopsy or ipsilateral salpingo-oophorectomy) are recommended for masses larger than 6 cm, with complex features or associated with ascites. These procedures, performed during the second trimester, aim to achieve an accurate histological diagnosis and reduce complications such as miscarriage, torsion, rupture, or delayed malignancy diagnosis (10).

Depending on the gestational age, the stage of the tumor, and the decisions taken at a multidisciplinary consultation meeting, it is recommended that a joint meeting be organized with the family to discuss the different treatment options available. These options include terminating the pregnancy, waiting until the fetus is viable before giving birth, followed by overall therapeutic management, or continuing the pregnancy while starting chemotherapy.

Radical treatment consists of total hysterectomy with bilateral adnexectomy, and possibly infragastric omentectomy if conditions allow. For primary tumors, a hemicolectomy or even a total colectomy may be performed for colonic tumors, while surgery will depend on the location of the tumor with the anal sphincter, with a safety margin of 2 cm for rectal tumors. Systemic chemotherapy is also a key component of treatment, as adjuvant or palliative therapy when the tumor is unresectable (9).

Following the results of the study conducted by Yang et al., their recommendations propose that if a tumor is detected before the 20th week of pregnancy, termination of pregnancy followed by surgery should be considered as a means to prevent the progression of the disease. Conversely, if the diagnosis is made after the 20th week of pregnancy, treatment can be delayed until the 32nd week of gestation to allow for adequate fetal maturation (11).

According to the conclusions of the study conducted by McLean et al., early tumors or tumors presumed to be curable detected between the 20th and 27th weeks of pregnancy should be treated by immediate hysterotomy and resection. On the other hand, if the tumor is diagnosed after 27 weeks, treatment can be deferred until a cesarean section at 32 weeks, accompanied by resection of the tumor (10).

Prognosis in cases of cancer during pregnancy is influenced by various factors, such as the patient's age, parity, tumor stage, timing of diagnosis, and gestational term. Early diagnosis of cancer at an operable stage is essential to improve prognosis. According to Pellino et al. review, which examined 119 patients across 79 papers, the average survival of mothers was 36 months (9). Additionally, Kocián et al. review reported a one-year survival rate of 78.1 % for mothers (12).

4 Conclusion

The presence of KT during pregnancy represents a real challenge for doctors, as the associated clinical symptoms are often confused with those of the pregnancy itself, making early diagnosis more difficult. As a result, tumors are often detected at an advanced stage, making treatment considerably more complicated. This case highlights the difficulties associated with diagnosis and the many ethical issues that arise in the treatment and management of malignant tumors during pregnancy.

Abbreviations

KT Krukenberg tumors

CRC Colorectal cancer

Consent

Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.

Ethical approval

“Ethical authorisation was not required for this case report by the Ethics Committee of the Mohammed V Military Training Hospital in Rabat, Morocco, as it concerned only one patient and did not involve any experimental or invasive procedures. The patient gave written informed consent for his personal and medical information to be used in this report”.

Funding

None.

Author contribution

BS, A B, HE, HM were responsible for the patient's diagnosis and clinical management., A B and SB wrote the manuscript. JK contributed to the analysis, supervision, writing, reviewing, and editing of the manuscript for intellectual content. All authors have read and approved the final manuscript.

Guarantor

The corresponding author is the guarantor of submission.

Research registration number

The name of the registry: researchregistry.com/ the hyperlink to the registration: https://www.researchregistry.com/browse-the-registry#home/ the unique identifying number of the study: researchregistry.

Declaration of competing interest

The authors declare no conflict of interest.

Acknowledgements

None.

Availability of data and materials

None.
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