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Is Diagnostic Hysteroscopy Protected for the Investigation of Kind II Endometrial Most cancers? A Retrospective Cohort Evaluation


Study Objective

Although hysteroscopy can be used for assessing the uterine cavity in women with suspected endometrial cancer (EC), it remains controversial as a procedure because it can potentially enhance the metastatic spread of cancer cells. Moreover, it is important to assess this hypothesis for type II EC, a more aggressive phenotype that usually presents with endometrial atrophy and has worse prognosis. Thus, we aimed to assess the prevalence of positive peritoneal cytology in women with type II EC who underwent hysteroscopy as a diagnostic tool and to determine the factors associated with patient relapse/survival.


Retrospective cohort analysis (2002-2017)


Tertiary, academic hospital

Patients or participants

127 women with type II EC


Diagnostic hysteroscopy (HSC) (n=43) or dilation/curettage (D&C) (n=84).

Measurements and Main Results

Primary endpoint was the frequency of positive peritoneal cytology. Survival curves were projected using the Kaplan-Meier method and compared using the log-rank test. Cox regression analysis with hazard ratio (HR) and 95% confidence intervals were calculated to assess the factors related with the disease-free survival (DFS) and the disease-specific survival (DSS). Advanced cancer stage and greater vascular invasion appeared more frequently in the D & C group (p=0.008 and p=0.04, respectively). Positive cytology was present in 2/43 (4.6%) women following HSC and in 9/84 (10.7%) following D&C (p=0.22). DFS and DSS curves did not statistically differ between the groups. Multivariate analysis for DFS showed that advanced cancer stage (III and IV) (HR=4.67 [2.34-9.34]; p<0.001) and advanced age (HR=1.08 [1.04-1.13]; p<0.001) were the factors associated with relapse. For DSS, advanced age (HR = 1.08 [1.05-1.12]; p<0.001), cancer stage III/IV (HR = 3.95 [2.18-7.15]; p<0.001), and vascular invasion (HR = 2.47 [1.34-4.54]; p=0.004) increased the risk of mortality.


Diagnostic HSC did not increase the rate of positive peritoneal cytology at the time of surgical staging in this cohort of women with type II EC and is probably as safe as D&C.



Endometrial cancer (EC) is the most common gynecological cancer in Europe and the United States, accounting for 7% of the new oncologic cases diagnosed in these countries each year [1]. In Brazil, EC is ranked as the eighth most common female cancer, and it is estimated that just over 6500 new cases will be diagnosed in 2020 [2]. According to the clinical and the endocrinological patterns, EC can be classified as type I or II. Type I (85% of the cases) is commonly characterized by the endometrioid histological subtype, a more indolent behavior, and a better prognosis; and is usually seen in obese patients. Type II, in contrast, includes more aggressive neoplasms (serous, clear cells, and carcinosarcomas) with a reserved prognosis [3–6] and affects patients with different phenotypes (non-obese, with atrophic endometrium).

Hysteroscopy (HSC) is considered the gold standard technique for diagnosing endometrial lesions. However, because a positive intrauterine pressure is exerted during its execution, the potential dissemination of the neoplastic cells to the depths of the myometrium, the vascular, the lymphatic spaces, and the peritoneal cavity is a concern [7]. The International Federation of Gynecology and Obstetrics (FIGO) does not consider the peritoneal cytology results for EC staging but recommends assessing the peritoneal fluid during surgical staging [8,9]. Therefore, cytology can play an important role in determining the prognosis of the patients with type II EC [10]. Moreover, we still do not know whether HSC can compromise the prognosis of women with type II EC.

Most studies, evaluating the presence of the neoplastic cells in peritoneal cytology, after confirming the diagnosis by hysteroscopy, as well as analyzing a change in prognosis in association with this alteration, are mostly conducted for type I EC [11–18]. To our knowledge, only one retrospective study, carried out by Chen et al., specifically evaluated the characteristics of women with type II EC [19]. Results from the studies evaluating type I EC cannot be extrapolated to the cases of type II EC due to the differences in prognosis and survival between these carcinomas. Thus, we sought to assess the prevalence of positive peritoneal cytology between the patients who underwent hysteroscopy or D & C, for the diagnosis of type II EC, and the factors associated with the survival curves between these diagnostic tools.


A retrospective cohort study was carried out, between 2002 and 2017, on the women with type II EC at a tertiary hospital affiliated with the University of Campinas. Ethical approval was provided by the Institutional Review Board (no. 3.313.097). Our hospital-based cancer registry system was assessed, and the records of the female patients, who were assigned the International Classification of Diseases 2013 code C54, were selected. We excluded those patients who did not undergo peritoneal cytology, had endometrioid histology, or synchronous malignancy, or were diagnosed by a method other than HSC or dilation/curettage (D&C).

D&C was performed using the traditional curettage biopsy method. HSC was performed with or without regional anesthesia (30‐degree STORZ® hysteroscope, Karl Storz GmbH, Tuttlingen, Germany) as per the institutional practice. The uterine cavity was then distended with either 0.9% sodium saline or 5% glucose solution to exert a pressure of 80 mmHg. Following HSC, Pipelle® biopsy (Cooper Surgical Inc., Trumbull, CT, USA) or hysteroscopic-directed biopsy was performed to obtain the samples of the endometrium for histopathology.

The following variables were obtained from the electronic medical records: age; age of menarche and/or menopause; parity; presence of comorbidities (arterial hypertension, diabetes mellitus), smoking status; body mass index (BMI – calculated by weight in kilograms divided by height squared in meters); clinical symptoms like presence of abnormal uterine bleeding (post or premenopausal bleeding or alteration in the menstrual pattern); surgical staging according to FIGO EC classification; histological type (serous, clear cells, mixed, carcinosarcoma, or others); and adjuvant treatment (whether radiotherapy and/or adjuvant chemotherapy were administered as per the institutional practices).

Primary outcome was the classification of peritoneal cytology into positive, negative, or inconclusive. About prognosis, disease-free time (DFS) and the disease-specific survival curves (DSS) were evaluated. DFS was defined as the time interval between the surgical EC staging and the first evidence of disease recurrence shown by another modality according to the physical or the complementary examinations (abdominal ultrasound, chest X-ray, computed tomography scan of the chest and abdomen) or death. As for DSS, the time elapsed between surgical staging and death caused by the cancer was considered, according to the time on the death certificate. For research purposes, patients were followed from the time of surgery until December 2019.

All cases of type II endometrial cancer were monitored at the institution from 2002 to 2017. Convenience sampling was used in this study. Continuous variables were described as mean and standard deviation, whereas the categorical variables were described as percentages. The Chi-square or the Fisher tests were used to compare the categorical variables between the groups, and the Mann–Whitney test was used for the continuous variables. A non-parametric distribution was considered for analysis. Survival analysis was performed using the Kaplan-Meier method and the log-rank test compared the disease-free and the specific survival times between the groups. Cox regression analysis was used to assess the factors related to survival and the disease-free time by calculating the hazard ratio with 95% confidence interval. A significance level of 5% was used and SAS version 9.4 (Cary, NC, USA) was used for the statistical analysis.


The overall database consisted of 1183 women with EC. After excluding the women with sarcomas or endometrioid carcinomas, 235 women with type II EC were selected. Of these, women who did not undergo surgery or for whom peritoneal cytology was not collected or recorded; and those who had another synchronous tumor at the time of diagnosis were excluded. The final sample comprised of 127 women who were diagnosed with EC type II by HSC (N = 43) or D&C (N = 84) (Figure 1).

Figure 1Flowchart of the pathway for selecting type 2 endometrial cancer patients for analysis

There was no difference in the clinical characteristics between the two groups. Positive cytology was found in 2/43 (4.6%) women following HSC and in 9/84 (10.7%) following D&C (p = 0.22). Advanced cancer stage and greater vascular invasion appeared more frequently in the D&C group (p = 0.008 and p = 0.04, respectively) (Table 1).

Table 1Comparison of clinical and pathological characteristics of women type 2 endometrial cancer according to the diagnostic procedure (n=127)

SD = standard deviation; BMI: Body Mass Index;

* Mann-Whitney test;

** Fisher’s exact test;

*** Chi-square test

Mean follow-up time was 53.6 months. Mean DFS and DSS periods were 48.55 ± 43.25 and 51.12 ± 41.95 months, respectively. Mean time interval between the diagnostic tests and surgical staging was 3.52 ± 2.08 months (HSC = 3.73 ± 2.06 months versus D&C = 3.42 ± 2.10 months; p = 0.222). There was no statistically significant difference in the survival curves between the groups (disease-free time, p = 0.572; specific survival time, p = 0.636) (Figure 2).

Figure 2Disease-free (A) and disease-specific survival (B) curves of women with type II endometrial cancer diagnosed by hysteroscopy or uterine curettage (n = 127)

Table 2 displays the univariate and the multivariate analyses of the factors associated with DFS. Crude analysis showed that advanced age (HR = 1.07 (1.03-1.12); p =

Table 2Factors associated with disease-free survival (DFS) within women type 2 endometrial cancer (n=127)

BMI: Body Mass Index; HR: Hazard Ratio; CI: confidence interval.

*Stepwise criteria for selection of variables.

Table 3 displays the same analysis, but for DSS. Advanced age, menopause duration, lower BMI, positive peritoneal cytology, advanced cancer stage, tumor size, vascular invasion, and adjuvant treatment were the variables that were associated with a higher risk of mortality during the univariate analysis. After removing the confounding factors, lymphovascular invasion (HR = 2.47 [1.34-4.54]; p = 0.004), advanced cancer stage (HR = 3.95 [2.18-7.15]; p

Table 3Factors associated with disease-specific survival (DSS) in women type 2 endometrial cancer (n=127)

BMI: Body Mass Index; HR: Hazard Ratio; CI: confidence interval.

*Stepwise criteria for selection of variables.

There was no association between the diagnostic tests (HSC and D&C) and the prognosis of type II endometrial cancer according to the disease-free and specific survival curves (HR = 1.7 [0.74-3.34]; p = 0.24 and HR = 1.55 [0.86-2.78]; p = 0.14, respectively) (Tables 2 and 3).


In this study, women diagnosed with type II EC through either HSC or D&C showed no difference in the rate of positive peritoneal cytology. These diagnostic methods were also not correlated with the results obtained by the DFS or DSS curves. Risk factors associated with worsening survival curves, after the multivariate analysis, were advanced age, advanced cancer stage, and lymphovascular invasion, which are similar to the factors found in other studies in the literature [13, 20]. These factors increased the rate of relapse and mortality among the women with type II EC.

Some studies found positive peritoneal cytology to be an independent factor that worsened the prognosis in the initial cases of EC [10, 14, 20–22]. Due to the use of a positive intrauterine pressure with HSC, there had been a concern that, when using this diagnostic tool, it might increase the risk of transferring the neoplastic cells to the peritoneal cavity. This could potentially increase the rate of disease recurrence and worsen the survival of the women, especially with EC type II, due to its more aggressive behavior. This concern arose when some studies reported findings diverging from the available evidence, regarding the higher incidence of positive peritoneal cytology after HSC [11, 12, 16–18, 23–28]. Obermair et al. performed one of the first studies that showed a significant increase in positive peritoneal cytology in women who underwent HSC compared to those who did not (12.2% versus 2.5%, p = 0.04) [24]. Other studies reinforced the result that HSC would increase the risk of positive peritoneal cytology [12, 16, 25, 26]. A meta-analysis of almost 3000 women with type I and II EC found a higher rate of positive peritoneal cytology in the group that underwent HSC compared to the group that did not [16].

However, other studies have supported the use of HSC as a safe diagnostic method for EC. Selvaggi et al. conducted a study on women undergoing either D&C, D&C followed by HSC, or HSC. They found no differences in the rates of positive peritoneal cytology or the presence of extrauterine micrometastasis between the diagnostic tests performed. This study used an infusion pressure, for distending the uterine cavity that ranged between 25 and 50 mmHg [18]. A randomized clinical trial with 140 women with type I EC, where half of them underwent diagnostic HSC with an infusion pressure of around 35-40 mmHg prior to the surgical treatment while the other half did not, showed no difference regarding the presence of positive peritoneal cytology between the groups [11]. These studies suggest that HSC performed at low pressures does not change the status of peritoneal cytology [11, 18]. Similarly, a meta-analysis observed that when HSC was performed with an infusion pressure greater than or equal to 100 mmHg, there was a trend toward finding an increased rate of positive peritoneal cytology [12]. Our results did not show increased rates of positive peritoneal cytology in women with type II EC who underwent HSC compared to those who underwent D&C, even though the latter procedure does not require a positive intrauterine pressure during its execution.

Regarding the influence of the diagnostic tools on DFS and DSS, our results showed that HSC and D&C were statistically equivalent for the women with type II EC. Other studies also point toward the safety of the usage of HSC. Cicinelli et al. found no difference in the risk of recurrence between the group that underwent HSC and the group that did not [11]. Although Chang et al. found a higher rate of positive peritoneal cytology in the HSC group, there was no difference when assessing the survival or the recurrence rates [16]. Another study analyzed a database of almost 2000 women with type I and II EC and found no association between HSC and the disease progression, risk of dissemination, or increased mortality [29]. In 2019, a study evaluated 1300 women with stage I EC and after following them for an average of 52 months, found that the disease-free time, specific survival, or overall survival did not worsen in those who underwent HSC [28].

One may hypothesize that the behavior of the neoplastic cells in the peritoneal cavity, when introduced iatrogenically by HSC, may differ than when these cells invade spontaneously due to the disease progression [10, 25, 26]. It is suggested that even though the neoplastic cells may be transferred to the peritoneal cavity during HSC, this is only transient, with cytology becoming negative after some time, as these tumor cells would not become viable implants [14].

Most studies investigating the role of HSC on the prognosis of EC have been conducted for EC type I patients. Similar to our study, the only study focusing on type II EC was carried out by Chen et al. [19]. They found a high incidence (30%) of positive peritoneal cytology in women undergoing HSC, which differs from our study where the highest prevalence of positive peritoneal cytology was found in the D&C group. However, regarding the prognosis of these women, our results were similar to the findings of this study, where no difference was found in DFS and DSS between the groups after a mean follow-up duration of 66 months [19].

Despite having no statistical significance, our study found a higher frequency of positive peritoneal cytology in the D&C group (10.7%) rather than in the HSC group (4.6%). This can be explained by the fact that the D & C group comprised of the women with endometrial cancer at a more advanced stage and with lymphovascular invasion.

In our study, endometrial biopsies were performed by Pipelleࣨ after HSC or by the biopsy forceps through the operating hysteroscope that allows for the performance of directed biopsies. The literature describes new tools that can be safely used to perform endometrial biopsies, such as biopsy snake grasper sec. Vitaleࣨ (Centrel S.r.l, Ponte San Nicolo, Padua, Italy) and Myosureࣨ tissue removal system (Hologic, Marlborough, MA, USA), the latter of which can also be used to excise polyps and fibroids [30,31]. It should be remembered that HSC is a diagnostic procedure that can be performed in an outpatient setting without anesthesia. In case of difficulties in accessing the cavity, painful symptoms can be avoided by using pharmacological agents, such as local anesthetics and non-steroidal anti-inflammatory drugs, or non-pharmacological resources such as music [32, 33].

The strengths of this study include the large period over which the retrospective cohort was analyzed and the long follow-up duration after the diagnosis of these patients. This is the second study available in the literature, to our knowledge, which addressed the role of HSC for type II EC, with the difference that it evaluated the rate of positive cytology as the primary outcome. Furthermore, we excluded only a short number of cases due to missing data. Our results suggest that HSC is a safe diagnostic procedure. It neither causes an increase in the rate of positive peritoneal cytology, nor is it associated with a change in the survival or the disease-free time. It is also not associated with additional risks, such as uterine perforation, that can be caused by a completely blind procedure like D&C. We chose not to perform a multivariate analysis with the associated factors for peritoneal cytology because we wanted to observe the survival curves from both diagnostic tools, and they did not have any statistically significant differences between them.

It is worth mentioning that a retrospective cohort has its limitations, such as the inability to control the exposure to the risk factors for an accurate outcome assessment. Another limitation is the inability to confirm whether the infusion pressure that was generated during HSC was 80 mmHg or not. Despite this being a protocol in our service, we did not compare the level of the positive pressure with the rate of positive peritoneal cytology. Due to this, we were unable to compare our findings with the studies that analyzed the potential risks of different levels of positive pressures. Moreover, a possible selection bias in this study may exist because HSC is not a procedure available in all the scenarios worldwide, especially in underdeveloped or developing countries with socioeconomic disparities. Thus, older women or those patients with more exuberant vaginal bleeding may have been assisted in centers where D & C is the procedure of choice, to diagnose the causes of abnormal uterine bleeding and younger women, with mild hemorrhagic symptoms, would have been referred to the tertiary institutions so that they could undergo HSC. Finally, as this sample was collected from a public health system, it could explain the delay of three months for the referral to the specialist for treatment.


HSC did not increase the rate of positive peritoneal cytology, analyzed at the time of surgical staging, and the difference in the rates of recurrence and survival did not exist between the two diagnostic procedures. These findings might suggest that HSC is a safer option for diagnosing type II EC.


We would like to thank Helymar da Costa Machado, statistician from Women´s Hospital (CAISM) for the statistical analysis of this study.


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Article Info

Publication History

January 5,

Received in revised form:
December 31,

November 23,

Publication stage

In Press Journal Pre-Proof


Conflicts of interest: The authors declare no conflicts of interest.

Funding: There was no funding or financial support for this study.

Précis: Diagnostic HSC did not increase the rate of positive peritoneal cytology when compared to uterine curettage for type 2 endometrial cancer




© 2021 Published by Elsevier Inc. on behalf of AAGL.


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