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 Table of Contents  
REVIEW ARTICLE
Year : 2018  |  Volume : 2  |  Issue : 2  |  Page : 120-127

A Retrospective Review of 10 Cases of Villoglandular Papillary Adenocarcinoma of the Uterine Cervix Including One with Successful Pregnancy


1 Laboratory of Reproductive Immunology, Obstetrics and Gynecology Hospital of Fudan University, Shanghai 200011, China
2 Department of Pathology, Obstetrics and Gynecology Hospital of Fudan University, Shanghai 200011, China
3 Department of Obstetrics and Gynecology, Shanghai General Hospital, Shanghai Jiao Tong University, Shanghai 201620, China
4 Department of Cervix, Obstetrics and Gynecology Hospital of Fudan University, Shanghai 200011, China
5 Department of Gynecology, Obstetrics and Gynecology Hospital of Fudan University; Key Laboratory of Female Reproductive Endocrine Related Disease, Shanghai 200011, China
6 Department of Gynecology, Obstetrics and Gynecology Hospital of Fudan University, Shanghai 200011, China

Date of Submission15-Apr-2018
Date of Web Publication4-Oct-2018

Correspondence Address:
Jun Shao
Obstetrics and Gynecology Hospital of Fudan University, 419, Fangxie Road, Shanghai 200011
China
Xiao-Yong Zhu
Obstetrics and Gynecology Hospital of Fudan University, 419, Fangxie Road, Shanghai 200011
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2096-2924.242755

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  Abstract 


Objective: Villoglandular papillary adenocarcinoma (VGPA) of the uterine cervix is a subtype of cervical adenocarcinoma. In the present study, we summarized the clinical features of VGPA of the uterine cervix and discussed the potential indications for a conservative treatment.
Methods: A retrospective review of clinical characteristics and treatment aspects of 10 patients with VGPA at the Obstetrics and Gynecology Hospital of Fudan University was conducted between January 2007 and December 2016. Almost all of the existing 40 English papers on “villoglandular papillary adenocarcinoma [title/abstract]” identified from PubMed were obtained. Clinical data from these papers were analyzed in terms of age, International Federation of Gynecology and Obstetrics (FIGO) stage, recurrence rate, mortality, and conservation treatment aspects.
Results: The median age of 10 patients with VGPA was 40 years. All cases had Stage IB 1 disease. Seven patients underwent human papillomavirus examinations, which revealed 6 positive and 1 negative case(s) of infection. Six patients underwent ThinPrep cytologic tests, which revealed 4 patients with atypical glandular cells, 1 with a high-grade squamous intraepithelial lesion, and 1 who tested negative for intraepithelial malignancy. None of the patients had lymph node metastases. During the 6–114 months of follow-up, no disease recurrence or death occurred. Of note, one patient who received conservative treatment successfully became pregnant.
Conclusions: VGPA can be detected at an early FIGO stage with excellent prognosis. For young patients who do not exhibit poor prognosis factors, conservative treatment may be the first treatment choice based on overall assessment of clinical conditions.

Keywords: Cervix Cancer; Conservative Treatment; Lymph Node Metastasis; Pregnancy; Villoglandular Papillary Adenocarcinoma


How to cite this article:
Wei CY, Qu YQ, He YY, Wang Q, Zhu XY, Shao J. A Retrospective Review of 10 Cases of Villoglandular Papillary Adenocarcinoma of the Uterine Cervix Including One with Successful Pregnancy. Reprod Dev Med 2018;2:120-7

How to cite this URL:
Wei CY, Qu YQ, He YY, Wang Q, Zhu XY, Shao J. A Retrospective Review of 10 Cases of Villoglandular Papillary Adenocarcinoma of the Uterine Cervix Including One with Successful Pregnancy. Reprod Dev Med [serial online] 2018 [cited 2018 Dec 13];2:120-7. Available from: http://www.repdevmed.org/text.asp?2018/2/2/120/242755




  Introduction Top


Cervical adenocarcinoma (AC), which accounts for 10–30% of all cervical cancers, is characterized by poor prognosis.[1] As a rare subtype of AC, villoglandular papillary adenocarcinoma (VGPA) of the uterine cervix is distinguished from common types of AC based on its excellent prognosis, infrequent lymphovascular space invasion (LVSI), and lymph node (LN) metastasis.[2] Histologically, the features of VGPA are exophytic proliferation, papillary architecture, and mild-to-moderate cellular atypicality.[3] Clinically, the predominant symptoms observed in patients with VGPA are contact bleeding and abnormal vaginal bleeding (AVB).[4] The clinical International Federation of Gynecology and Obstetrics (FIGO) stages of patients are mainly early stage. Although some researchers have proposed that conservative treatment for VGPA may be effective, there are no guides for evidence-based decisions regarding conservative treatment for VGPA. In fact, conservative treatments were administered to few patients with VGPA who desired to maintain fertility.[5],[6],[7],[8],[9],[10],[11],[12],[13],,[14]

In this study, we report 10 cases with VGPA, including one with successful pregnancy; the cases were analyzed with the aim of summarizing the clinical features of VGPA of the uterine cervix and discussing the potential indications for conservative treatment of patients with VGPA. To our knowledge, approximately 179 cases of VGPA have been reported in the English literature.[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40] We reviewed and analyzed data of these cases to present various features of VGPA, which may help us in acquiring more knowledge on VGPA.


  Methods Top


Electronic medical records of patients with cervical cancer were retrospectively collected from the Obstetrics and Gynecology Hospital of Fudan University (Shanghai, China) between January 2007 and December 2016. We selected patients who were suspected of having VGPA preoperatively and analyzed the data of these patients. Approval was obtained from the Institutional Review Boards of the Obstetrics and Gynecology Hospital of Fudan University.

The criteria used for diagnosing VGPA were based on the morphological characteristics as defined by the World Health Organization.[15] All slides from every patient were re-examined to confirm the diagnosis. Two expert pathologists (XR Z and YQ Q) reviewed the pathologic slides without previous knowledge of the clinical outcomes.

In total, the medical data of 25 patients with preoperatively suspected or confirmed VGPA were obtained in our study. Excluding patients who received treatment at other hospitals or were lost to follow-up, 18 patients were enrolled in this retrospective study. Eight patients without VGPA postoperatively were excluded, and 10 patients were definitively diagnosed with VGPA finally. Clinical profiles consisted of age, presenting symptoms, reproductive history, gynecological examination (cervix) results, clinical FIGO stage, contraceptive method, ThinPrep cytologic test (TCT) results, human papillomavirus (HPV) infection, preoperative diagnosis, LVSI, requirement for further fertility, treatment, LN metastasis, adjuvant therapy, postoperative diagnosis, poor prognostic factor(s), length of follow-up (months), and outcomes.

We searched for “villoglandular papillary AC [title/abstract]” in the PubMed database and collected the most relevant papers. Data from these papers were analyzed to present more details about VGPA profiles.

All analyses were performed using IBM SPSS Statistics 22 (IBM Inc., Armonk, New York, USA) and Numbers version 3.2.2 (Apple Inc., Cupertino, California, USA).


  Results Top


We searched electronic medical records and identified 7,251 inpatients with cervical cancer between January 1, 2007, and December 31, 2016, in the Obstetrics and Gynecology Hospital of Fudan University. Among them, 968 patients (13.35%) had cervical adenocarcinoma, which was consistent with rates reported in the literature.[1] We collected the medical records of 25 patients who were preoperatively suspected or postoperatively diagnosed with VGPA. Of these, 8 patients were preoperatively diagnosed with VGPA based on biopsy, 4 underwent surgery at our hospital and were postoperatively diagnosed with VGPA, and 4 received therapy at other hospitals or were lost to follow-up and were not included in our study. For another 16 patients, confirming preoperative diagnosis of VGPA or usual-type endocervical adenocarcinoma (UEA) based on biopsy was difficult. After surgery, 5 of 16 patients were definitively diagnosed with VGPA, 8 were diagnosed with UEA, and 3 were lost to follow-up. In addition, one patient was suspected with endometrial carcinoma Stage IA. With limited numbers of cases, we found that postoperative diagnosis was more likely to be precise than preoperative diagnosis, although there was no significant difference [Table 1]. Finally, a total of 10 patients were confirmed to have been diagnosed with VGPA.
Table 1: Fisher's exact test of the difference between pre- and postoperative diagnoses in our retrospective study

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Clinical profiles of villoglandular papillary adenocarcinoma

In our retrospective study, the mean age of 10 patients was 40 years, ranging from 24 to 55 years. AVB was the main presenting symptom (6 of 10 patients). All patients presented with friable, papillary, or polypoid masses [Figure 1]a. The papillae were tall and thin and contained fibrovascular stroma focally infiltrated by lymphocytes and plasma cells [Figure 1]b. Six of these ten patients underwent TCTs: 4 patients had atypical glandular cells (AGCs), 1 had a high-grade squamous intraepithelial lesion (HSIL), and 1 tested negative for intraepithelial malignancy. In addition, 7 of 10 patients underwent HPV examinations: 6 patients had a high-degree HPV infection and 1 tested negative. All patients were classified as Stage IB 1. Regarding contraception, records of 6 patients were obtained, with 3 using intrauterine devices and 3 using condoms. Regarding treatments, 2 patients underwent loop electrosurgical excision procedures (LEEPs), 2 patients underwent laparoscopic total hysterectomy, and 6 patients underwent radical hysterectomy with or without pelvic LN dissection. Among them, 1 patient received concurrent chemoradiation therapy, and 1 patient received chemotherapy. Besides 5 patients who were postoperatively diagnosed with VGPA alone, 2 patients were diagnosed with VGPA combined with adenocarcinoma in situ (AIS), 1 patient with VGPA combined with AIS and HSIL, 1 patient with VGPA combined with UEA, and 1 patient with VGPA combined with HSIL. All cases involved <50% myometrial invasion. Among them, lesions in 2 patients who underwent LEEPs were confined to the mucosal layer, and other cases did not include superficial muscular infiltration. In addition, 2 of them exhibited LVSI, but none of them had LN metastases. The follow-up duration was between 6 and 114 months. None of the patients died or exhibited recurrence of VGPA [Table 2] and [Table 3].
Figure 1: Histopathologic characteristics of VGPA of the uterine cervix. (a) Vegetant neoformation in cervical ectopic area (case 10). (b) Thin and tall, well-formed papillary structures and mild nuclear atypia of VGPA of the uterine cervix (case 1) (H and E, ×200 and ×400). (c) Well-differentiated VGPA of the cervix was diagnosed during pregnancy (H and E, ×200 and ×400) and appearance of colposcopic examination results (case 6). VGPA: Villoglandular papillary adenocarcinoma.

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Table 2: Clinical features of 10 patients with VGPA

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Table 3: Lesions invasion profile of 10 patients with VGPA

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One patient with villoglandular papillary adenocarcinoma who became successfully pregnant

Among these 10 patients with VGPA, we reported one patient who received conservative treatment and became successfully pregnant later [patient 6 in [Table 2]]. She was 24-year-old maiden, and her presenting symptom was contact bleeding. On gynecological examination, a polyp measuring 2 cm × 1.5 cm in size was detected in the cervix of the uterus. The results of the TCT revealed AGCs and negativity for HPV infection. Moreover, the ovaries and uterus were normal in the B-ultrasonic examination. She then underwent a colposcopic examination and polyp excision promptly [Figure 1]c. The pathological diagnosis of the cervical neoplasm was VGPA with P53(+), carcinoembryonic antigen(+), progesterone receptor(++), Ki-67(+), estrogen receptor(+), and P16(+). Magnetic resonance imaging (MRI) and an enhancement scan of the pelvic cavity showed that the signal in the cervix of the uterus was less homogeneous and multiple Nessler's cyst of the cervix. Considering her intense desire for further fertility and her clinical condition, she was scheduled to undergo LEEP. No cancer cells were identified in the resected specimens, and the postoperative diagnosis was chronic cervicitis. After LEEP, the patient regularly consulted her doctor and no recurrence of VGPA was detected. In addition, positron emission tomography/computed tomography findings were normal. To be noted, she received oral metformin (0.5 g bid. oral) in the first 2 months for the diagnosis of polycystic ovarian syndrome with insulin resistance. After 1 year, the patient became pregnant. The duration of the pregnancy was normal, and she delivered a healthy baby by cesarean section in the 38th week of gestation. Seven months postpartum, the baby was healthy, and the patient was in good condition without evidently abnormal TCT, HPV, colposcopic examination, or pelvic MRI findings.

In conclusion, since the first report of 13 cases of VGPA involving excellent prognosis in 1989,[25] approximately 40 related English papers have been published, comprising approximately 179 cases.[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40] Most existing reports of VGPA are of descriptive cases and literature reviews. However, few basic research reports, which explore potential mechanisms that participate in the pathogenesis of VGPA, have been published. Several studies have demonstrated that HPV infection might have a relationship with VGPA,[2],[4],[12] and in our retrospective study, 7 of 10 patients underwent HPV examinations and 6 of them tested positive for HPV infection. However, the number of cases is insufficient. Although numerous researchers have described elaborate mechanisms of HPV that participate in the development of cervical cancer, whether VGPA involves similar mechanisms requires further research. In addition, the oral contraceptive pill (OCP) is another factor that may be associated with VGPA;[14] in fact, this may be debatable. Except for Jones et al.'s[14] study in which 15 of 24 patients with VGPA had taken OCPs, several other reports recently showed that few patients take OCPs for certain durations before being diagnosed with VGPA.[2],[4],[5] Consistently, none of the patients with VGPA had a history of taking OCPs before the diagnosis in our study [Table 2].

In the clinical profile for VGPA, young age, early FIGO stage (mainly IB 1), low incidence of recurrence, low mortality rate, and excellent prognosis are the main features of VGPA [Figure 2].
Figure 2: Clinical features of VGPA of the uterine cervix. (a) Numbers and percentages of different age groups among patients with VGPA. Total: 150 cases. (b) Numbers and percentages of patients with VGPA who received or did not receive conservative treatment. Total: 179 cases. (c) Numbers of different FIGO stages in different age groups of patients with VGPA. (d) Details of recurrence cases in FIGO stage (numbers and percentages). (e) Details of mortality in FIGO stage (numbers and percentage). Total: 107 cases of c-e. CON: Conservative treatment; NON CON: Not conservative treatment; STAGE: FIGO stage: RECURRENCE (%), recurrence percentage; NO: Number; VGPA: Villoglandular papillary adenocarcinoma; FIGO: International Federation of Gynecology and Obstetrics.

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Based on reports of 150 (the total number of existing cases is 179; however, the age information of 24 cases in Reference 14 and 5 cases in Reference 41 were not available, so these 29 cases were excluded when analyzing the age composition of patients with VGPA) cases of VGPA,[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39] we analyzed the percentage of different age groups among patients with VGPA. As shown in [Figure 2]a, 38% (57/150) were aged 31–40 years, closely followed by 31% (47/150) aged 41–50 years, 14% (21/150) aged 21–30 years, 10% (15/150) aged 51–60 years, and 7% (10/150) aged older than 60 years.

Although many reports proposed that VGPA was associated with early FIGO stage,[2],[3],[5],[6],[7],[8],[9],[10],[11] none of these studies had analyzed the age composition of existing cases in relationship with FIGO stages. Here, we summarized numbers of different FIGO stages in different age groups.[2],[4],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24] To be noted, the FIGO stage of cervical cancers before the year 2000 was not subdivided as IB 1 and IB 2, so those reported cases were not included in the analysis, and the total number was 107 cases. As shown in [Figure 2]b, 70 of 107 cases of VGPA were classified as FIGO Stage IB 1. Among them, there were 32 and 25 patients aged 31–40 years and 41–50 years, respectively. Therefore, the number of Stage IB 2 cases was 10, the same number of Stage IIB cases. Besides, a number of cases of other stages were sporadically several.

In addition, 12 of 179 (6.70%) patients exhibited recurrence of disease and 9 of 179 (5.02%) died in the review of reported cases. In the retrievable data of 107 reported cases [Figure 2]c, the recurrence ratios of Stages IB 1, IB 2, IIB, IIIB, and IIIC were 4/70 (5.71%), 1/10 (10.0%), 2/10 (20.0%), 2/3 (66.67%), and 1/1 (100.0%), respectively; the mortality ratios of Stages IB 1, IB 2, IIB, and IIIB were 2/70 (2.86%), 1/10 (10.0%), 2/10 (20.0%), and 3/3 (100.0%), respectively [Figure 2]d. As previously established, LN metastasis is one of the most important poor prognosis factors, which may correlate with cancer recurrence.[12],[19] Indeed, about 14 of 179 patients with VGPA harbored LN metastasis. Among them, most exhibited recurrence of VGPA. In our study, 2 of these 10 patients presented with LVSI, but none of them had LN metastases. During the 6–114 months of follow-up, none of the patients died or exhibited recurrence of VGPA.

Despite these conditions, most patients underwent radical operations for treatment, and only about 19 of 179 patients (10.61%) received conservative treatment when diagnosed with VGPA.[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40] Among them, 2 of these patients were pregnant and 17 patients expressed a desire for further fertility, and finally, 6 patients delivered babies. Moreover, about 5 gestational women received expectant management when diagnosed with VGPA based on biopsy and delivered babies via cesarean section along with radical resection. As shown, 8 patients underwent cesarean sections and 2 patients underwent vaginal delivery. The mean age was 30.17 years (range: 26–34 years). In fact, none of them developed recurrence or died due to VGPA [Table 4]. In our retrospective study, the 2 patients who received conservative treatment had expressed a desire for further fertility and their lesions were confined to the mucosal layer. Besides, lesions in the other 8 patients were superficial, which may indicate that the infiltration depth of VGPA is likely to be superficial, which is consistent with that reported in other papers.[14],[25]
Table 4: Clinicopathological findings of patients who were pregnant or expressed the desire for further fertility when diagnosed with VGPA

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According to the findings described above, we considered whether overtreatment might occur in the therapy of patients with VGPA, which may be the reason underlying the low incidence and low level of recognition. Moreover, VGPA is indistinguishable from other gynecological cancers preoperatively, such as UEA.[2],[4],[7] In our retrospective study, the patient in case 1 was suspected with endometrial carcinoma Stage IA preoperatively and confirmed with VGPA postoperatively, which may suggest that definitive diagnosis is difficult for VGPA preoperatively. Although there are a limited number of cases of VGPA, postoperative diagnosis seemed to be more precise [Table 1]. To administer appropriate therapy, especially for conservative treatment, factors including age, FIGO stage, LVSI, depth of stromal invasion, resection margin invasion, simultaneous diseases (such as other gynecological cancers), LN metastasis, and feasible follow-up examination should be considered seriously.[20] In addition, evidence-based studies are essential for guiding the treatment of VGPA, especially for conservative treatment, which may be based on large samples and multiple centers.

In this study, we reported 10 cases of VGPA and reviewed a series of papers from the English literature that were related to VGPA. To our knowledge, conservative treatment may be the first treatment choice for patients with VGPA with early FIGO stage who are young and exhibit no other poor prognosis factors. To be noted, the overall assessment of patients' conditions and informed consent sufficiently before therapy are necessary, especially before initiating conservative treatment. For young patients with VGPA who desire further fertility, assisted reproduction technologies may be considered. Regular TCTs and HPV examinations are necessary for women's health.

Financial support and sponsorship

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Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Barbu I, Crăiţoiu S, Mărgăritescu C. Cervical adenocarcinoma: A retrospective clinicopathologic study of 16 cases. Rom J Morphol Embryol 2012;53:615-24.  Back to cited text no. 1
    
2.
Zhou QY, Chen HY, Yang SM, Li YH, Wu XQ. Villoglandular papillary adenocarcinoma of the uterine cervix: A report of 4 cases and a review of the literature. Oncol Lett 2016;11:837-41. doi: 10.3892/ol.2015.3944.  Back to cited text no. 2
    
3.
Collinet P, Prolongeau JF, Vaneecloo S. Villoglandular papillary adenocarcinoma of the uterine cervix. Eur J Obstet Gynecol Reprod Biol 1999;86:101-3. doi: 10.1016/S0301-2115(99)00047-0.  Back to cited text no. 3
    
4.
Zhao L, Xu T, Cui M, Fu Z. A retrospective review of 11 cases of villoglandular papillary adenocarcinoma of the uterine cervix and a review of the literature. Oncol Lett 2016;11:2164-8. doi: 10.3892/ol.2016.4172.  Back to cited text no. 4
    
5.
Takai N, Hayashita C, Nakamura S, Narahara H, Matsumoto H. A case of villoglandular papillary adenocarcinoma of the uterine cervix diagnosed during early pregnancy followed by successful term delivery. Case Rep Med 2010;2010:314547. doi: 10.1155/2010/314547.  Back to cited text no. 5
    
6.
Lavie O, Segev Y, Peer G, Gutterman E, Sagie S, Auslnader R. Conservative management for villoglandular papillary adenocarcinoma of the cervix diagnosed during pregnancy followed by a successful term delivery: A case report and a review of the literature. Eur J Surg Oncol 2008;34:606-8. doi: 10.1016/j.ejso.2007.05.014.  Back to cited text no. 6
    
7.
Korach J, Machtinger R, Perri T, Vicus D, Segal J, Fridman E, et al. Villoglandular papillary adenocarcinoma of the uterine cervix: A diagnostic challenge. Acta Obstet Gynecol Scand 2009;88:355-8. doi: 10.1080/00016340902730359.  Back to cited text no. 7
    
8.
Falcón O, García R, Lubrano A, Morín JC, Andujar M. Successful term delivery following conservative management for villoglandular papillary adenocarcinoma of the uterine cervix: A case report. Gynecol Oncol 2006;101:168-71. doi: 10.1016/j.ygyno.2005.09.059.  Back to cited text no. 8
    
9.
Hoffman JS, Bazzurini L, Laird L, Murphy JC, Magriples U, Lewis J. Term delivery following conservative treatment for villoglandular papillary adenocarcinoma of the uterine cervix: Report of a case and analysis of the literature. Gynecol Oncol 2001;81:310-3. doi: 10.1006/gyno.2001.6129.  Back to cited text no. 9
    
10.
Bouman A, Oosterhuis GJ, Naudin ten Cate L, van Doorn GA. Villoglandular papillary adenocarcinoma of the cervix. Beware of a wolf in sheep's clothing. Eur J Obstet Gynecol Reprod Biol 1999;87:183-9. doi: 10.1016/S0301-2115(99)00106-2.  Back to cited text no. 10
    
11.
Borgo G, Feyles E, Gaglio A, Tagliani L, Andrion A. Villoglandular papillary adenocarcinoma of the uterine cervix: Report of a case. Tumori 1998;84:717-9. doi: 10.1177/030089169808400621.  Back to cited text no. 11
    
12.
Kim HJ, Sung JH, Lee E, Ahn S, Song SY, Choi CH, et al. Prognostic factors influencing decisions about surgical treatment of villoglandular adenocarcinoma of the uterine cervix. Int J Gynecol Cancer 2014;24:1299-305. doi: 10.1097/IGC.0000000000000197.  Back to cited text no. 12
    
13.
Novotny DB, Ferlisi P. Villoglandular adenocarcinoma of the cervix: Cytologic presentation. Diagn Cytopathol 1997;17:383-7. doi: 10.1002/(SICI)1097-0339(199711)17:5<383::AID-DC13>3.0.CO;2-J.  Back to cited text no. 13
    
14.
Jones MW, Silverberg SG, Kurman RJ. Well-differentiated villoglandular adenocarcinoma of the uterine cervix: A clinicopathological study of 24 cases. Int J Gynecol Pathol 1993;12:1-7. doi: 10.1097/00004347-199301000-00001.  Back to cited text no. 14
    
15.
Scully RE, Bonfiglio TA, Kurman RJ, Silverberg SG, Wilkinson EJ. Histological typing of female fenital tract tumors. World Health Organization International Histological Classification of Tumors. 2nd ed. New York: Springer-Verlag; 1994. p. 44.  Back to cited text no. 15
    
16.
Guzin K, Sahin S, Goynumer G, Eroğlu M, Usta A, Ozel N. A rare coexistence of villoglandular papillary adenocarcinoma of the uterine cervix and Brenner tumor of the ovary. Case Rep Obstet Gynecol 2014;10:1-3. doi: 10.1155/2014/342040.  Back to cited text no. 16
    
17.
Takai N, Hayashita C, Nakamura S, Narahara H, Matsumoto H. Villoglandular papillary adenocarcinoma of the uterine cervix diagnosed during pregnancy. Eur J Gynaecol Oncol 2010;31:573-4.  Back to cited text no. 17
    
18.
Giordano G, D'Adda T, Gnetti L, Merisio C, Gabrielli M, Melpignano M. Villoglandular adenocarcinoma of the cervix: Two new cases with morphological and molecular study. Int J Gynecol Pathol 2007;26:199-204. doi: 10.1097/01.pgp.0000228141.01964.e7.  Back to cited text no. 18
    
19.
Lataifeh IM, Al-Hussaini M, Uzan C, Jaradat I, Duvillard P, Morice P. Villoglandular papillary adenocarcinoma of the cervix: A series of 28 cases including two with lymph node metastasis. Int J Gynecol Cancer 2013;23:900-5. doi: 10.1097/IGC.0b013e31828efcaa.  Back to cited text no. 19
    
20.
Fadare O, Zheng W. Well-differentiated papillary villoglandular adenocarcinoma of the uterine cervix with a focal high-grade component: Is there a need for reassessment? Virchows Arch 2005;447:883-7. doi: 10.1007/s00428-005-0030-3.  Back to cited text no. 20
    
21.
Hagiwara T, Kaku T, Kobayashi H, Wake N, Saito T. Well-differentiated villoglandular adenocarcinoma of the uterine cervix: Assessment of cytological features by histological subtypes. Acta Cytol 2013;57:61-8. doi: 10.1159/000342917.  Back to cited text no. 21
    
22.
Rubesa-Mihaljević R, Vrdoljak-Mozetic D, Ostojić DV, Stemberger-Papić S, Sindik N, Krasević M. Villoglandular papillary adenocarcinoma of the uterine cervix with aggressive clinical course – A case report. Coll Antropol 2010;34:291-4.  Back to cited text no. 22
    
23.
Utsugi K, Shimizu Y, Akiyama F, Umezawa S, Hasumi K. Clinicopathologic features of villoglandular papillary adenocarcinoma of the uterine cervix. Gynecol Oncol 2004;92:64-70. doi: 10.1016/j.ygyno.2003.10.020.  Back to cited text no. 23
    
24.
Dede M, Deveci G, Deveci MS, Yenen MC, Goktolga U, Dilek S, et al. Villoglandular papillary adenocarcinoma of the uterine cervix in a pregnant woman: A case report and review of literature. Tohoku J Exp Med 2004;202:305-10. doi: 10.1620/tjem.202.305.  Back to cited text no. 24
    
25.
Young RH, Scully RE. Villoglandular papillary adenocarcinoma of the uterine cervix. A clinicopathologic analysis of 13 cases. Cancer 1989;63:1773-9. doi: 10.1002/1097-0142(19900501)63:9<1773::AID-CNCR2820630920>3.0.CO;2-J.  Back to cited text no. 25
    
26.
Hurteau JA, Rodriguez GC, Kay HH, Bentley RC, Clarke-Pearson D. Villoglandular adenocarcinoma of the cervix: A case report. Obstet Gynecol 1995;85:906-8. doi: 10.1016/0029-7844(94)00418-D.  Back to cited text no. 26
    
27.
Takeuchi M, Matsuzaki K, Bando Y, Sakaki M, Furumoto H, Harada M. Magnetic resonance manifestations of villoglandular papillary adenocarcinoma of the uterine cervix with a fern-leaf-like appearance. Magn Reson Med Sci 2014;13:267-70. doi: 10.2463/mrms.2013-0078.  Back to cited text no. 27
    
28.
Choi Y, Kim H, Choi H, Hwang D, Choe G, Chung JH, et al. Liquid-based cytology of villoglandular adenocarcinoma of the cervix: A report of 3 cases. Korean J Pathol 2012;46:215-20. doi: 10.4132/KoreanJPathol.2012.46.2.215.  Back to cited text no. 28
    
29.
Gurumurthy M, Lahiri R, Kennedy AM, Miller I, Parkin DE. A case of villoglandular papillary adenocarcinoma of the cervix with vaginal skip metastasis. Gynecol Oncol Case Rep 2011;1:1-3. doi: 10.1016/j.gynor.2011.10.001.  Back to cited text no. 29
    
30.
Lai CY, Chen JR, Chen YJ, Hsu CH, Wang TW, Yang YC, et al. Villoglandular adenocarcinoma of the uterine cervix: An analysis of 12 clinical cases. Int J Gerontol 2011;5:49-52. doi: 10.1016/j.ijge.2011.01.009.  Back to cited text no. 30
    
31.
Nagai N, Hirata E, Kusuda T, Mukai K, Arihiro K, Ohama K. Villoglandular papillary adenocarcinoma of the uterine cervix responding to neoadjuvant chemotherapy with docetaxel and cisplatin: A case report. Int J Gynecol Cancer 2005;15:1187-90. doi: 10.1111/j.1525-1438.2005.00186.x.  Back to cited text no. 31
    
32.
Heron DE, Axtel A, Gerszten K, Amortegui A, Kelley J, Comerci J, et al. Villoglandular adenocarcinoma of the cervix recurrent in an episiotomy scar: A case report in a 32-year-old female. Int J Gynecol Cancer 2005;15:366-71. doi: 10.1111/j.1525-1438.2005.15231.x.  Back to cited text no. 32
    
33.
Garcea A, Nunns D, Ireland D, Brown L. A case of villoglandular papillary adenocarcinoma of the cervix with lymph node metastasis. BJOG 2003;110:627-9. doi: 10.1046/j.1471-0528.2003.02097.x.  Back to cited text no. 33
    
34.
Utsugi K, Shimizu Y, Akiyama F, Hasumi K. Villoglandular papillary adenocarcinoma of the uterine cervix with bulky lymph node metastases. Eur J Obstet Gynecol Reprod Biol 2002;105:186-8. doi: 10.1016/S0301-2115(02)00146-X.  Back to cited text no. 34
    
35.
Rodriguez A, Isaac MA, Hidalgo E, Márquez B, Nogales FF. Villoglandular adenocarcinoma of the vulva. Gynecol Oncol 2001;83:409-11. doi: 10.1006/gyno.2001.6372.  Back to cited text no. 35
    
36.
Jones MW, Kounelis S, Papadaki H, Bakker A, Swalsky PA, Woods J, et al. Well-differentiated villoglandular adenocarcinoma of the uterine cervix: Oncogene/tumor suppressor gene alterations and human papillomavirus genotyping. Int J Gynecol Pathol 2000;19:110-7. doi: 10.1097/00004347-200004000-00003.  Back to cited text no. 36
    
37.
Chang WC, Matisic JP, Zhou C, Thomson T, Clement PB, Hayes MM. Cytologic features of villoglandular adenocarcinoma of the uterine cervix: Comparison with typical endocervical adenocarcinoma with a villoglandular component and papillary serous carcinoma. Cancer 1999;87:5-11. doi: 10.1002/(SICI)1097-0142(19990225) 87:1<5::AID-CNCR2>3.0.CO;2-D.  Back to cited text no. 37
    
38.
Stanley-Christian H, Heim BK, Hines JF, Hall KL, Willett GD, Barnes WA. Villoglandular adenocarcinoma of the cervix: A report of three cases and review of the literature. Gynecol Oncol 1997;66:327-30. doi: 10.1006/gyno.1997.4747.  Back to cited text no. 38
    
39.
Kaku T, Kamura T, Shigematsu T, Sakai K, Nakanami N, Uehira K, et al. Adenocarcinoma of the uterine cervix with predominantly villogladular papillary growth pattern. Gynecol Oncol 1997;64:147-52. doi: 10.1006/gyno.1996.4539.  Back to cited text no. 39
    
40.
Khunamornpong S, Siriaunkgul S, Suprasert P. Well-differentiated villoglandular adenocarcinoma of the uterine cervix: Cytomorphologic observation of five cases. Diagn Cytopathol 2002;26:10-4. doi: 10.1002/dc.10028.  Back to cited text no. 40
    


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