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Synchronous mucinous metaplasia and neoplasia of the female genital tract (SMMN‑FGT): A case report and literature review

  • Authors:
    • Hongliang Xu
    • Yong Chen
    • Shuguang Zhou
    • Caixia Zhao
    • Qin Wang
    • Man Tang
    • Weiqin Zhang
    • Heping Zhang
  • View Affiliations

  • Published online on: December 19, 2022
  • Article Number: 73
  • Copyright: © Xu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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The present study reported a case of Synchronous Mucinous Metaplasia and Neoplasia of the Female Genital Tract (SMMN‑FGT), which occurred in a 47‑year‑old woman. The patient complained of pelvic mass during a physical examination a month ago. Ultrasound examination found an anechoic spot in the left ovary and several anechoic spots were detected in the cervix. The patient underwent left adnexectomy and the left ovarian frozen section revealed a mucinous borderline tumor. Total abdominal hysterectomy and right salpingo‑oophorectomy were subsequently performed. Microscopically, multifocal mucinous lesions were involved in the female genital tract, including bilateral ovarian mucinous borderline tumor, cervical and endometrial mucinous adenocarcinoma and the bilateral fallopian tube epithelium showed mucinous metaplasia. Immunohistochemistry revealed that the tumor cells of the ovary, cervix and endometrium expressed MUC6, exhibiting features of gastric‑type differentiation. The Ki‑67 proliferative index was ~10‑70%. Cumulative evidence established SMMN‑FGT as the final histopathological diagnosis with International Federation of Gynecology and Obstetrics stage I. Following surgery, the patient received a course of pelvic radiotherapy and survived for 16 months.


Synchronous Mucinous Metaplasia and Neoplasia of the Female Genital Tract (SMMN-FGT) is a multifocal mucinous lesion that occurs simultaneously in the female genital tract and was first described by Mikami et al (1). SMMN-FGT rarely occurs; ~35 cases have been reported in the literature (1-11). SMMN-FGT demonstrates a spectrum of morphological features, ranging from metaplasia without nuclear or architectural abnormalities to invasive mucinous adenocarcinoma, including minimal deviation adenocarcinoma (MDA) of the cervix and usually with gastric differentiation. Whether the disease process is the multifocal independent occurrence or the widespread dispersal from a single lesion is still controversial. The present study reported the clinical data, histological morphology and immunohistochemistry of this case and is expected to provide a further reference for the clinicopathological characteristics of the disease and the basis for its diagnosis and treatment.

Case study

The patient was a 47-year-old married woman who complained of a pelvic mass during a physical examination a month ago (February, 2021). The preoperative transvaginal ultrasound displayed multiple inhomogeneous hypoechoic echoes without obvious blood flow signals in the uterine myometrium (the largest one on the right uterine wall, which occludes the right ovary; Fig. 1A and B). There was a 52x52x33 mm well-circumscribed anechoic spot in the left ovary without an obvious blood flow signal (Fig. 1C). Several anechoic spots were detected in the cervix, with a maximum diameter of 8 mm. The endometrium measured ~5 mm in thickness. Cervical liquid-based cytology (Thinprep cytologic test, TCT) was negative for intraepithelial lesions or malignant lesions and the high-risk HPV test was negative. The patient underwent left adnexectomy; a frozen section of the left ovarian revealed a mucinous borderline tumor. The patient underwent a rapid cytological examination of the peritoneal washing fluid and no tumor cells were found. Intraoperative examination of the appendix and other digestive tract organs showed no obvious abnormality. Total abdominal hysterectomy and bilateral salpingo-oophorectomy were subsequently performed.

Gross presentation

The removed bilateral ovaries were measured 50x45x25 mm (left) and 32x20x15 mm (right) (grossly view of the specimen) in size and were multicystic tumors without conspicuous papillae in the cyst wall. The uterus body measured ~100x45x25 mm in size. Multiple grey-white nodules were in the intramural and subserosa of the uterus with a diameter of 2-48 mm. The thickness of the endometrium was 2-5 mm. The cervical canal was measured ~35 mm in length and 3 0 mm in diameter, with multiple cervical cystic lesions scattered in the endocervix. The bilateral fallopian tubes were grossly unremarkable.

Microscopic examination

Bilateral ovarian tumors have similar histological features and contain multiple cysts lined by gastric-type mucinous epithelium showing variable degrees of stratification, tufting and villous or slender filiform papillae. Tumor cells are generally low-grade nuclear atypia. Mitotic activity is predominantly present in crypts and less prominent on the luminal surface (Fig. 2A). The bilateral fallopian tube mucosal epithelium showed focal mucinous metaplasia (Fig. 2B).

The cervical lesion in the internal cervical canal displayed a well-differentiated mucinous adenocarcinoma with focal superficial invasion and is surrounded by lobular endocervical glandular hyperplasia (LEGH; Fig. 2C). The tumor was confined to the cervix without vascular invasion and did not invade beyond the lower uterus. The tumor cells with abundant clear pale eosinophilic cytoplasm and distinct cell borders. The cytoplasm contained neutral mucins, which stained pale pinkish-red. (Fig. 2D).

The mucinous endometrial tumor showed a nodular expansive growth pattern and invaded the superficial myometrium (3/15 mm) without vascular invasion (Fig. 2E). It had similar morphological features to the cervical tumor, such as abundant cytoplasm containing mucins and atypical mitoses were present but inconspicuous (Fig. 2F). The background endometrium displayed hyperplasia.

Immunohistochemical findings

Immunohistochemically, ovarian tumor cells expressed MUC6, CK7, PAX8 (Fig. 3A-C), a Ki-67 proliferation index of ~70% (Fig. 3D) and were negative for ER, PR, CDX-2, CK20 (data not shown). Cervical tumor cells expressed MUC6 (Fig. 3E), were negative for P16 and P53 (Fig. 3F and G) and had a Ki-67 proliferation index of ~50% (Fig. 3H). Endometrial tumor cells expressed MUC6 (Fig. 3I), were negative for ER, PR (Fig. 3J and K), P16 and P53 (data not shown) and the Ki-67 proliferation index was ~10% (Fig. 3L).

The patient underwent gastroscopy and colonoscopy following surgery and no gastrointestinal lesions were found. Combined with the clinical visualization, histological features and immunohistochemical results, the primary diagnosis was ascertained as SMMN-FGT by the International Federation of Gynecology and Obstetrics stage I (12), including mucinous borderline tumor (MBT) of the bilateral ovaries, gastric-type cervical adenocarcinoma (GCA), endometrial mucinous adenocarcinoma and fallopian tubes epithelium mucinous metaplasia. The secondary diagnosis was multiple uterine leiomyomas. The patient was been referred to a course of pelvic radiotherapy followed surgery. The follow-up showed that the patient was alive and disease-free at 16 months after surgery.


Mucinous lesions that occur in two or more sites of the female genital tract simultaneously, including the cervix, endometrium, ovary, or fallopian tube, are rare. Occasionally, the involvement of the urethral orifice and peritoneum has also been reported (2). These rare mucinous lesions are termed SMMN-FGT. The distinguishing feature of SMMN-FGT is that all tumors co-occur and exhibit features of gastric-type differentiation, such as expression of MUC6 and/or HIK-1083. Most of the cervix lesions are GCA which is usually called MDA when it is extremely well-differentiated. The 5th WHO Classification of female genital tract tumors (13) classifies it as HPV-independent adenocarcinoma due to its different pathogenesis from traditional cervical adenocarcinoma. Some patients are also accompanied by Peutz-Jeghers syndrome (14). Molecular genetics may be related to the mutation of STK11(15) and KRAS (16).

To the best of the authors' knowledge, ~35 cases of SMMN-FGT have been reported in the literature (Table I) (1-11). The age of the patients ranged from 33-83 years (mean, 51 years old). The clinical manifestations of SMMN-FGT are not exclusive. Most patients complained of irregular vaginal bleeding, vaginal discharge, or abdominal discomfort; some patients exhibit atypical glandular cells on cervical cytology. The patient in the present study was a middle-aged woman diagnosed with a pelvic mass by physical examination but without other symptoms. The negative cytology result may be that the materials could not be effectively collected because of the mucinous lesions confined to the internal cervical canal. In addition, in traditional cervical cancer screening (cervical cytology combined with HPV test) it is easy to miss the lesions because it is HPV-independent.

Table I

Clinical and pathological features of 35 patients with SMMN-FGT.

Table I

Clinical and pathological features of 35 patients with SMMN-FGT.

Author, yearCaseAgeSymptomsCervixEndometriumTubeOvaryRemarksFIGOTreatmentFollow-up(Refs.)
Giles et al, 1994148Irregular vaginal bleedingMucinous adenocarcinomaPapillary mucinous adenocarcinomaMucinous carcinoma in situInvasive mucinous adenocarcinoma, mucinous cystadenomaN/AN/ATAH + BSO + RTDisease-free survival (9 months)(8)
Jackson- York et al, 1992248Irregular vaginal bleedingPapillary mucinous adenocarcinoma, AISNormalPapillary mucinous carcinoma (left)Metastatic adenocarcinoma (left)N/AN/ATAH + BSON/A(7)
Anjarwalla et al, 2007365Urinary incontinence 18 monthsCervical agenesisMucinous metaplasiaPseudopyloric metaplasiaAtypical mucinous epithelium (left)Entire genital epithelial surface replaced by müllerian epithelialN/ATAH + BSODisease-free survival (20 months)(9)
Nagahama et al, 2013452Increased vaginal dischargeLEGHMucinous metaplasiaNormalNormalPeritoneal cytology revealed several mucin- containing epithelial clustersN/ATAH + BSO, paclitaxel- carboplatin 5 coursesN/A(3)
Mangili et al, 2004541Left adnexal mass, abdominal painMDASimplex hyperplasia with a component of clear cell metaplasiaMucinous metaplasiaMBT (left)PJSN/ATAH + BSODisease-free survival (21 months)(6)
Ikeda et al, 2015673AVD, lower abdominal painMucinous adenocarcinomaMucinous adenocarcinomaNormalMBTExternal urethral meatus neoplasmN/ATAH + BSO, partial omentectomy, appendectomy and mesenteric and external urethral meatus neoplasm resection, chemotherapyLung metastases were found after 6 months(2)
Lu et al, 2019757AVDGCAMucinous metaplasiaMBT (left)NormalHPV 16 positiveN/ATAH + BSON/A(4)
Xu et al, 2021844Abdominal massGastric-type mucinous hyperplasiaMucinous metaplasiaNormalMucinous cystadenomaKRAS G13D mutationN/ATAH + right salpingo- oophorectomyN/A(10)
Gu et al, 2018937-70 Average 54AVD, abdominal massGastric-type mucinous hyperplasiaLEGHMucinous metaplasia (right)Mucinous cystadenom a (left)N/AN/ATAH + BSODisease-free survival (2-34 months) without relapse(5)
 10 AVDAIS, LEGH, ALEGHAIS, LEGH, ALEGHNormalMucinous cystadenomaN/AN/ATAH + BSO  
 11 AVDGCAGastric-type adenocarcinoma, mucinous metaplasia, MDAMucinous metaplasia (right)NormalNormalN/ATAH + BSO + PEL, RT, chemotherapy  
 12 Abdominal massGCA, LEGH, ALEGHLEGH, ALEGHMucinous metaplasia (left)Mucinous cystadenomaN/AN/ATAH + BSO, chemotherapy  
 13 AVDGCA, MDAGastric-type adenocarcinoma, mucinous metaplasia, MDAMucinous metaplasia (right)NormalTumor invades lymph nodes and blood vesselsN/ATAH + BSO + PEL + PAN, RT, chemotherapy  
 14 AVDGCA, MDAGastric-type adenocarcinoma, mucinous metaplasia, MDAAIS (left)NormalVagina invadingN/ATAH + BSO + PEL, RT, chemotherapy  
 15 AVDAIS, LEGH, ALEGHAIS, LEGH, ALEGHMucinous cystadenoma (right)NormalN/AN/ATAH + BSO  
Mikami et al, 20091647AGC on Pap smearsMDA, AIS, LEGHMucinous adenocarcinoma, mucinous metaplasiaMucinous cystadenomaNormalPeritoneal washing positiveIATAH + BSODisease-freel surviva (36 months)(1)
 1760Abdominal painMDA, AIS, LEGHMucinous metaplasia, LEGHMBTMBTN/AIATAH + BSODisease-free survival (37 months) 
 1865AGC on Pap smearsMDA, AIS, LEGHMucinous metaplasiaMucinous metaplasiaNormalPeritoneal washing positiveIATAH + BSO, chemotherapyDisease-free survival (102 months) 
 1962AGC on Pap smearsMDA, AIS, LEGHMucinous adenocarcinoma, mucinous metaplasiaMBTNormalVagina invadingIIATAH + BSO + PEL + PAN, chemotherapyDied after 62 months 
 2039AGC on Pap smearsAIS, LEGHMucinous adenocarcinoma, mucinous metaplasiaNormalNormalN/ANATAH + BSO + PEL, chemotherapyDisease-free survival (13 months) 
 2183Ovarian cystNormalMucinous metaplasia, LEGHMBTMBTPeritoneal washing positiveICTAH + BSODisease-free survival (25 months) 
Chen et al, 20222256AVDCervicitisALEGHMucinous metaplasia (right)Mucinous metaplasia (left)N/AN/ATAH + BSODisease-free survival (80 months)(11)
 2337AVDALEGH, GCA in situMucious metaplasiaGastric adenomatous metaplasia (left)Mucinous cystadenomaN/AN/ATAO + BSODisease-free survival (75 months) 
 2441AVD, Ovarian cystGCAGastric-type adenocarcinomaNormalMucinous cystadenomaN/AN/ATAO + BSODisease-free survival (64 months) 
 2536AGC on Pap smearsMDAMDAMucinous carcinoma (right)Mucinous carcinoma (right)Vaginal wall (+), Parametrium (+)N/ARH + RSO + BPLND + OMT + AEDisease-free survival (60 months) 
 2649Ovarian cystALEGH, GCAGastric-type adenocarcinomaGastric-type adenocarcinoma (left)MBT (left)N/AN/ATAH + LSODisease-free survival (52 months) 
 2754AVDGCAGastric-type adenocarcinomaMucinous metaplasia (Gastric type, right)Brenner tumor (right)N/AN/ATAH + BSO + EPH + BPLND + PALNDDied after 36 months 
 2833AVBLEGHMucinous metaplasia, gastric-typeMucinous metaplasia, gastric-typeReserved, not checkedN/AN/ATAH + BSDisease-free survival (43 months) 
 2946Ovarian cystALEGHALEGHNormalMucinous cystadenoma (right)N/AN/ATAH + RSODisease-free survival (42 months) 
 3046AVDMDAMDANormalMBT (left)N/AN/ATAH + BSODisease-free survival (36 months) 
 3139AVDLEGHMucinous metaplasia, Gastric-typeNormalReserved, not checkedN/AN/ATAH + BS + BBODisease-free survival (36 months) 
 3251Ovarian cystLEGH, ALEGHLEGHLEGH (right)Mucinous cystadenoma (right)N/AN/ATAH + RSODisease-free survival (33 months) 
 3337AVBLEGHLEGHNormalReserved, not checkedN/AN/ATAH + BSDisease-free survival (29 months) 
 3452AVD/AVBGCAMucinous metaplasiaMucinous metaplasia (left)NormalVaginal wall (+)N/ARH + BSO + BPLNDDisease-free survival (14 months) 
Hongliang et al, 20223547Abdominal massGCAMucinous adenocarcinomaMucinous metaplasiaMBTN/AIATAH + BSO, RTDisease-free survival (16 months)Present case

[i] AVD, abnormal vaginal drainage; AVB, abnormal vaginal bleeding; AGC, atypical glandular cell; GCA, gastric-type cervical adenocarcinoma; AIS, adenocarcinoma in situ; LEGH, lobular endocervical glandular hyperplasia; ALEGH, atypical lobular endocervical glandular hyperplasia; MDA, minimal deviation adenocarcinoma; MBT, mucinous borderline tumor; TAH, total abdominal hysterectomy; BSO, bilateral salpingo-oophorectomy; PEL, pelvic lymphadenectomy, PAN, para-aortic lymphadenectomy; RT, radiotherapy; RH, radical hysterectomy; RSO, right salpingo-oophorectomy; PALND, para-aortic lymph node dissection; OMT, omentectomy; AE, appendectomy; LSO, left salpingo-oophorectomy; EPH, extensive parametrial hysterectomy; BPLND, bilateral pelvic lymph node dissection; BS, bilateral salpingectomy; glands; BBO, biopsy of both ovaries; N/A, not available.

Among the described cases, 23 cases showed gastric-type cervical mucinous adenocarcinoma and three cases without cervical mucinous lesions. 15 cases of endometrial lesions manifested as mucinous adenocarcinoma, nine cases were mucinous metaplasia and eight showed occasional villoglandular growth associated with LEGH. A total of 12 cases of fallopian tube lesions were mucinous metaplasia, five cases were mucinous carcinomas and four cases were mucinous borderline tumors. A total of seven cases of the ovarian lesions were mucinous borderline tumors, eight were mucinous cystadenoma and three were ovarian mucinous carcinoma. Among the 35 cases, 21 cases involved three sites of the female genital tracts and 10 cases involved four sites. In the patient in the present study, mucinous lesions involved four sites of the genital tracts, including the cervix, endometrium, bilateral ovaries and fallopian tubes. The cervix and endometrium were gastric-type adenocarcinomas, bilateral ovaries were MBT and bilateral fallopian tube epithelium were mucinous metaplasia.

The primary differential diagnosis of SMMN-FGT is metastatic ovarian mucinous adenocarcinoma. Notably, Metastatic ovarian mucinous adenocarcinoma closely resembles primary or mucinous borderline tumors and requires close macroscopic and microscopic observations combined with clinical information for accurate identification. The features of metastatic ovarian mucinous adenocarcinoma from cervical cancer were described by Young and Scully (17) including i) The ovarian tumor may metastasize from cervical cancer if the ovarian and cervical cancer occur at a similar time; ii) tumors are usually present in bilateral ovaries, iii) tumor implants visible on the surface of the ovary, iv) cervical and ovarian tumors have similar histological features, v) Cervical tumor usually infiltrates deep myometrium, vi) cervical tumor widely spread, vii) tumor invades lymph nodes and blood vessels and viii) deficiency of mucous metaplasia of the fallopian tubes or endometrial lining. Moreover, well-differentiated mucinous adenocarcinoma of the digestive tract, such as well-differentiated mucinous adenocarcinoma of the gallbladder, metastases to the cervix and ovary, possesses similar morphological features to cervical MDA and ovarian mucinous cystadenoma. In the present case, the mucinous tumors existed on cervical, bilateral ovaries and endometrium with similar histological characteristics, but the lower uterine segment, ovarian surface and blood vessels were without tumor invasion, which demonstrated the ovarian tumor was not metastasized from the cervical tumor. Moreover, the endometrial and cervical tumors were limited to the superficial myometrium. Combined with the clinical features, imaging findings, histology and immunohistochemistry, the ovarian, endometrial and cervical tumor occurred simultaneously. Cumulative evidence established SMMN-FGT as the final histopathological diagnosis.

Treatment of SMMN-FGT is usually based on the stage of the co-existing adenocarcinoma. Total abdominal hysterectomy (TAO) and bilateral salpingo-oophorectomy (BSO) are sufficient for early staging. Most of the 22 reported cases were treated with TAO and BSO. Some patients received adjuvant radiotherapy and chemotherapy after surgery. The prognosis of patients is mainly related to the staging of the most severe lesions (1). One patient died 62 months after surgery because the lesions invaded the vaginal wall and reoccurred 9 months after surgery. The follow-up of other patients ranged from 2-102 months and they survived disease-free. In the present case, the patient underwent a rapid cytological examination of the peritoneal washing fluid during the operation and the results showed that no tumor cells were found. The appearance of the resected tumor was limited to the ovary and the surface of the ovary was smooth and no tumor was observed. Therefore, no omentectomy was performed during the clinical operation, but this may also be where treatment is inadequate. Finally, the patient underwent TAO, BSO and a course of radiotherapy following surgery. The patient was disease-free 16 months following the completion of the therapy.

The present study reported a case of SMMN-FGT that occurred in a 47-year-old woman, including the clinical symptoms, ultrasound display, gross appearance, microscopic examination and immunohistochemical findings. However, there are some limitations to the present study. First, the images of an MRI or CT scan on the pelvis before surgery were not taken as the preoperative clinical diagnosis was of a benign ovarian cyst. In addition, the tumors of the cervix and endometrium were inconspicuous, so the present study collected a large number of cervical and endometrial tissues for diagnosis, only to find superficial tumor lesions and that the gross specimen was damaged, so the present study lacked an image displaying the gross characteristics of this rare tumor.

The present study presented a case of SMMN-FGT, which existed in the cervix, endometrium and bilateral annex. Immunohistochemistry showed that the tumor cells were positive for gastric-type marker MUC6. Further studies are of great significance to characterize clinical features of this rare disease for differential diagnosis and effective therapy.


Not applicable.


Funding: The present study was supported by Anhui Medical University Funding Project (grant no. 2020xkj066).

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Authors' contributions

HX contributed to the original conception of the study, data analyses and wrote the manuscript. YC acquired hematoxylin and eosin staining, immunohistochemical and ultrasound images. SZ performed the surgery and contributed to the acquisition of data. CZ and QW provided pathological diagnosis. MT performed tissue specimen collection. WZ prepared hematoxylin and eosin and immunohistochemical sections. HZ performed the analysis of the data and revised the manuscript. All authors read and approved the final manuscript. HX and YC confirmed the authenticity of all the raw data.

Ethics approval and consent to participate

Ethics approval was obtained from the Ethics Committee of Anhui Medical University (approval no. 81220058) and Anhui Province Maternity and Child Health Hospital (approval no. YYLL2022-2020xkj066-11-1.0).

Patient consent for publication

Written informed consent for publication was obtained from patient, including the patient's data and images.

Competing interests

The authors declare that they have no competing interests.



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Xu H, Chen Y, Zhou S, Zhao C, Wang Q, Tang M, Zhang W and Zhang H: Synchronous mucinous metaplasia and neoplasia of the female genital tract (SMMN‑FGT): A case report and literature review. Exp Ther Med 25: 73, 2023
Xu, H., Chen, Y., Zhou, S., Zhao, C., Wang, Q., Tang, M. ... Zhang, H. (2023). Synchronous mucinous metaplasia and neoplasia of the female genital tract (SMMN‑FGT): A case report and literature review. Experimental and Therapeutic Medicine, 25, 73.
Xu, H., Chen, Y., Zhou, S., Zhao, C., Wang, Q., Tang, M., Zhang, W., Zhang, H."Synchronous mucinous metaplasia and neoplasia of the female genital tract (SMMN‑FGT): A case report and literature review". Experimental and Therapeutic Medicine 25.2 (2023): 73.
Xu, H., Chen, Y., Zhou, S., Zhao, C., Wang, Q., Tang, M., Zhang, W., Zhang, H."Synchronous mucinous metaplasia and neoplasia of the female genital tract (SMMN‑FGT): A case report and literature review". Experimental and Therapeutic Medicine 25, no. 2 (2023): 73.