Abstract
BACKGROUND:
The role of endocervical curettage (ECC) in the diagnosis of cervical intraepithelial neoplasia (CIN) is a controversial topic.
OBJECTIVES:
Investigate the role of ECC in the diagnosis of CIN in human papillomavirus (HPV) positive patients.
DESIGN:
Retrospective
SETTING:
A tertiary training and research hospital
PATIENTS AND METHODS:
This study included patients who were referred for colposcopy between 2018-2022 because of abnormal screening results. ECC results, age, cytology, HPV status, and colposcopic impression of the patients were extracted from the medical records. Multinomial logistic regression analyses were performed to identify factors that could predict CIN on ECC.
MAIN OUTCOME AND MEASURES:
The likelihood of high-grade squamous intraepithelial lesions (HSIL) in ECC in patients with cervical biopsy results of normal and low-grade squamous intraepithelial lesion (LSIL).
SAMPLE SIZE:
2895 women
RESULTS:
In patients with normal and LSIL cervical biopsy results, HSILs were detected in 6.7% of ECC results. There was no difference in the detection rates of CIN in ECC among groups with smear results negative for intraepithelial lesions or malignancy (NILM), atypical squamous cells of undetermined significance (ASC-US), and LSIL. The likelihood of HSIL being observed in ECC was 2.2 times higher in patients with HPV16. The probability of LSIL disanois was 2.3 times higher in women aged 50-59 years and 2.8 times higher in women ≥ 60 years compared to the reference group of <30 years. The probability of LSIL was 2.3 and HSIL by ECC was 2.2 times higher in both age categories (P<.012 and P=.032, respectively) than the reference group of <30 years.
CONCLUSION:
Regardless of colposcopic findings, ECC should be performed in patients with smear results of NILM who are positive for HPV16, in patients with smear results of ASC-US and LSIL who are positive for any oncogenic type of HPV and in patients 50 and above with any result of smear or any oncogenic HPV type.
LIMITATIONS:
We did not have the components of the HPV types in mixed groups.
INTRODUCTION
Cervical cancer is the fourth most common cancer among women worldwide but has a declining incidence in developed countries due to screening programs.1 Cervical thin-layer liquid-based cytology alone, human papillomavirus (HPV) detection alone or cytology combined with HPV detection is performed as the primary screening.2–4 Subsequently, women who have abnormal screening results are referred for colposcopic evaluation, and histopathological specimens of the lesions, including colposcopically directed biopsy and/or endocervical curettage (ECC) might be taken. Because millions of women undergo colposcopic evaluation due to abnormal screening results each year, the colposcopic evaluation is at the center of screening programs. However, there are some problems at the colposcopy step in relation to colposcopy practice and obtaining of histopathological specimens. Because visualizing the endocervical status of a lesion is difficult and the experience of colposcopists vary, many clinicians are often required to perform ECC to help rule out an occult, high-grade squamous intraepithelial or worse lesion (HSIL+).
On the other hand, ECC is a painful procedure that adds to the overall cost; therefore, it should not be performed without a justified reason, such as yielding appreciable diagnostic information. The need for ECC remains controversial because of the lack of consensus on when to perform ECC. While there are country-specific consensus guidelines for ECC, there is no consensus guideline that can be used worldwide.5
Particularly in cases of negative for intraepithelial lesions or malignancy (NILM), atypical squamous cells of undetermined significance (ASC-US) and low-grade squamous intraepithelial lesion (LSIL); there was a lack of clear data about when to perform ECC. In this study we aimed to investigate the role of ECC in the diagnosis of cervical intraepithelial neoplasia (CIN) in HPV positive patients who had cytologic results of NILM, ASC-US or LSIL.
PATIENTS AND METHODS
This retrospective study encompassed all consecutive patients referred to the Izmir Tepecik Research Hospital, Department of Gynecology and Obstetrics, between 2018 and 2022, based on abnormal co-test findings (HPV testing + cytology), who underwent colposcopic biopsy and ECC. This study protocol was reviewed and approved by the Ethics Committee of Health Sciences University, Faculty of Medicine, İzmir Tepecik Education and Research Hospital (2023/01-15, 07/02/2023). The need for informed consent was waived by the Ethics Committee of Health Sciences University, Faculty of Medicine, İzmir Tepecik Education and Research Hospital (2023/01-15, 07/02/2023). This study was performed in line with the principles of the Declaration of Helsinki.
Age and other demographic data, and menopausal state was obtained via electronic medical records. We included all patients with positive HPV testing results and cytology findings with NILM, ASC-US and LSIL. All colposcopy, biopsy and ECC procedures were performed at the same experienced colposcopy unit. In our clinic's routine practice, colposcopy-directed cervical biopsy is performed, and alongside biopsy, ECC was also conducted for every patient.
The study included patients who underwent colposcopy for the first time, while those who had a control colposcopy were excluded. Patients with cytology results of ASC-H, HSIL, squamous cell carcinoma, atypical glandular cells not otherwise specified (AGC-NOS), atypical glandular cells-favor neoplasia (AGC-FN), adenocarcinoma in situ (AIS), and adenocarcinoma of the cervix (AC) were excluded. Patients were also excluded if they had a history of cervical physical therapy (ablation or cryosurgery), surgical operations (loop electrosurgical excision procedure, cold knife cone or hysterectomy) or pelvic radiotherapy.
Because we performed an ECC on every patient from whom we conducted a biopsy, regardless of whether the transformation zone was fully visible, we classified patients with features such as acetowhite staining indicative of CIN as abnormal, and those without any such findings as normal.
Patients for whom a comprehensive pathological evaluation could not be performed due to inadequate ECC material were also excluded from the study. HPV status was defined by subtypes as HPV16, 18 or other (high-risk non-16/18 HPV) and mixed substypes. The mixed group comprises various combinations involving HPV16, HPV18, and other subtypes. For instance, within this group, one patient may exhibit positivity for HPV16 alongside another subtype, while another patient may test positive for both HPV16 and 18. Additionally, there were cases where all three types were simultaneously detected in a single patient. Liquid-based Pap smear methods were used in the study. Pathological results were evaluated and interpreted by pathologists at our hospital according to the Lower Anogenital Squamous Terminology (LAST) system 2012.6
Analyses were performed using the IBM SPSS version 20 program (Armonk, NY, USA: IBM Corp). The percentage distribution of descriptive data are presented. The relationship between ECC results and individual and clinical characteristics was evaluated with the Pearson chi-suare Test. OR and 95% confidence intervals of subgroups of individual and clinical characteristics according to ECC result categories were calculated by multinomial logistic regression analysis (Table 4). In this analysis, the “benign” category of the ECC result was taken as the reference category. As a result of the analysis, if P<.05, the relationship between the variables was considered significant.
Table 4.
The relationship between endocervical curettage results and individual and clinical characteristics (multinomial logistic regression analysis).
| Variable | Endocervical curettage | |||||
|---|---|---|---|---|---|---|
| LSIL | HSIL | |||||
| OR | 95% Cl | P | OR | 95% Cl | P | |
| Age group | ||||||
| <30 (ref) | 1.0 | 1.0 | ||||
| 30–39 | 1.2 | 0.8; 2.0 | .376 | 1.4 | 0.8; 2.4 | .312 |
| 40–49 | 1.4 | 0.8; 2.0 | .203 | 1.8 | 1.0; 3.2 | .054 |
| 50–59 | 2.3 | 1.4; 3.8 | .001 | 2.2 | 1.2; 4.0 | .012 |
| ≥60 | 2.8 | 1.5; 5.1 | .001 | 2.2 | 1.1; 4.7 | .032 |
| Menopause | ||||||
| Premenopause (ref) | 1.0 | 1.0 | ||||
| Postmenopause | 1.9 | 1.6; 2.4 | .001 | 1.3 | 1.1; 1.7 | .016 |
| Colposcopy | ||||||
| Normal (ref) | 1.0 | 1.0 | ||||
| Abnormal | 0.9 | 0.7; 1.1 | 0.278 | 2.9 | 2.0; 4.4 | .001 |
| Smear | ||||||
| Benign (ref) | 1.0 | 1.0 | ||||
| ASC–US | 1.2 | 1.0; 1.4 | 0.138 | 1.2 | 0.9; 1.5 | .157 |
| LSIL | 1.0 | 0.7; 1.3 | 0.797 | 1.2 | 0.9; 1.7 | .165 |
| HPV subtype | ||||||
| HPV 16 | 0.9 | 0.7; 1.1 | .209 | 2.2 | 1.6; 2.9 | .001 |
| HPV 18 | 0.8 | 0.6; 1.2 | .358 | 0.6 | 0.3; 1.2 | .141 |
| Mix | 1.0 | 0.8; 1.3 | .855 | 1.8 | 1.3; 2.4 | .001 |
| HPV other (ref) | 1.0 | 1.0 | ||||
Reference category is benign.
RESULTS
We reviewed the records of 5286 patients, with 3063 having ASC-US, LSIL, or normal smear results. Among this group, 168 had inadequate ECCs. Our analysis focused on 2895 patients, while 2223 were excluded (Figure 1). The ECC results of 2895 women were examined. Age distribution, menopausal status, colposcopic appearances, HPV, smear, biopsy and ECC results are shown in Table 1. In the ECC results of patients with normal cervical biopsy results, the percentage of LSIL was 6.5% and HSIL 1.7% (Table 2). HSIL was detected by ECC in 5% of patients with LSIL cervical biopsy. In total, patients with normal and LSIL cervical biopsy results, HSIL was detected in 6.7% of ECC results.
Figure 1.
Patient flow diagram.
Table 1.
Descriptive characteristics of the patients.
| Variable | |
|---|---|
| Age group | |
| <30 | 157 (5.4) |
| 30–39 | 1033 (35.7) |
| 40–49 | 1087 (37.5) |
| 50–59 | 482 (16.6) |
| ≥60 | 136 (4.7) |
| Menopause | |
| Premenopause | 2069 (71.5) |
| Postmenopause | 826 (28.5) |
| Colposcopy | |
| Normal | 521 (18.0) |
| Abnormal | 2374 (82.0) |
| Pap smear | |
| Benign | 1528 (52.8) |
| ASC-US | 926 (32.0) |
| LSIL | 441 (15.2) |
| HPV subtypes | |
| HPV16 | 1063 (36.7) |
| HPV18 | 227 (7.8) |
| Mix | 782 (27.0) |
| HPV other | 823 (28.4) |
| Endocervical curettage | |
| Benign | 1981 (68.4) |
| LSIL | 537 (18.5) |
| HSIL | 377 (13.0) |
| Biopsy | |
| Benign | 476 (16.4) |
| LSIL | 1579 (54.5) |
| HSIL | 840 (29.0) |
| Total | 2895 (100.0) |
Data are number (percentage). LSIL: low-grade squamous intraepithelial lesion; HSIL: high-grade squamous intraepithelial lesions.
Table 2.
Distribution of endocervical curettage and cervical biopsy results.
| Endocervical curettage | ||||
|---|---|---|---|---|
| Benign | LSIL | HSIL | Total (n) | |
| Benign | 437 (91.8) | 31 (6.5) | 8 (1.7) | 476 |
| LSIL | 1072 (67.9) | 428 (27.1) | 79 (5.0) | 1579 |
| HSIL | 472 (56.2) | 78 (9.3) | 290 (34.5) | 840 |
| Total | 1981 (68.4) | 537 (18.5) | 377 (13.0) | 2895 |
Data are number (percentage). LSIL: low-grade squamous intraepithelial lesion; HSIL: high-grade squamous intraepithelial lesions.
ECC results showed a significant relationship with all variables examined, except for pap-smear results (Table 3). In terms of the detection rates of CIN in ECC, no difference was found among the three groups with smear results of NILM, ASC-US, and LSIL. While the percentage of benign diagnoses decreased after the age of 50, the number of LSIL cases increased. In the post-menopausal period, the diagnosis of LSIL increased significantly, while the diagnosis of HSIL increased slightly. The rate of HSIL was significantly higher in women with abnormal colposcopy results compared to those with normal results. The probability of women aged 50-59 years to be diagnosed with LSIL was 2.3 times, and those over 60 years were 2.8 times more likely to be diagnosed with LSIL (Table 4). The probability of being diagnosed with HSIL was 2.2 times higher in both groups. Postmenopausal women are 1.9 times more likely to be diagnosed with LSIL and 1.3 times more likely to be diagnosed with HSIL. The probability of HSIL in the group with abnormal colposcopy results was 2.9 times higher than the group with normal results. There was no difference in the incidence of CIN by ECC between cases with smear results of NILM, ASC-US and LSIL, both in the group with normal and abnormal colposcopy results (Table 5). HPV16 positive patients were 2.2 times more likely to have HSIL in ECC.
Table 3.
Distribution of endocervical curettage results according to individual and clinical characteristics.
| Variable | Endocervical curettage | ||||
|---|---|---|---|---|---|
| Benign | LSIL | HSIL | Statistical analysis | ||
| n | %a | %a | %a | P | |
| Age group | |||||
| <30 | 157 | 77.1 | 14.0 | 8.9 | |
| 30–39 | 1033 | 72.3 | 16.4 | 11.3 | |
| 40–49 | 1087 | 68.8 | 17.1 | 14.1 | .001 |
| 50–59 | 482 | 59.8 | 25.1 | 15.1 | |
| ≥60 | 136 | 56.6 | 28.7 | 14.7 | |
| Menopause | |||||
| Premenopause | 2069 | 71.7 | 15.7 | 12.6 | .001 |
| Postmenopause | 826 | 60.2 | 25.7 | 14.2 | |
| Colposcopy | |||||
| Normal | 521 | 72.7 | 21.9 | 5.4 | .001 |
| Abnormal | 2374 | 67.5 | 17.8 | 14.7 | |
| Pap-smear | |||||
| Benign | 1528 | 69.8 | 18.1 | 12.1 | |
| ASC-US | 926 | 66.2 | 20.1 | 13.7 | .433 |
| LSIL | 441 | 68.3 | 17.0 | 14.7 | |
| HPV | |||||
| HPV16 | 1063 | 66.1 | 16.6 | 17.3 | |
| HPV18 | 227 | 75.8 | 18.5 | 5.7 | |
| Mix | 782 | 66.9 | 19.1 | 14.1 | .001 |
| HPV other | 823 | 70.8 | 20.7 | 8.5 | |
| Total | 2895 | 68.4 | 18.5 | 13.0 | |
Row percentage. Statistical analysis by chi-square test; LSIL: low-grade squamous intraepithelial lesion; HSIL: high-grade squamous intraepithelial lesions.
Table 5.
Distribution of endocervical curettage results according to colposcopy results and clinical features.
| Endocervical curettage (row percentage) | ||||||
|---|---|---|---|---|---|---|
| Benign | LSIL | HSIL | Statistical analysis | |||
| Chi-square | P | |||||
| Menopause | ||||||
| Normal | Premenopause | 79.2 | 16.5 | 4.3 | 21.716 | <.001 |
| Postmenopause | 60.0 | 32.6 | 7.4 | |||
| Abnormal | Premenopause | 70.2 | 15.6 | 14.2 | 26.080 | <.001 |
| Postmenopause | 60.2 | 23.8 | 16.0 | |||
| Smear | ||||||
| Normal | Benign | 73.1 | 21.6 | 5.3 | ||
| ASC-US | 67.3 | 25.8 | 6.9 | 6.277 | .179 | |
| LSIL | 82.3 | 15.2 | 2.5 | |||
| Abnormal | Benign | 69.1 | 17.3 | 13.7 | ||
| ASC-US | 66.0 | 18.9 | 15.1 | 4.582 | .333 | |
| LSIL | 65.2 | 17.4 | 17.4 | |||
| HPV subtypes | ||||||
| Normal | HPV16 | 74.9 | 19.8 | 5.4 | ||
| HPV18 | 83.0 | 14.9 | 2.1 | 12.994 | .043 | |
| Mix | 63.6 | 26.5 | 9.8 | |||
| HPV other | 74.9 | 22.3 | 2.9 | |||
| Abnormal | HPV 16 | 64.5 | 16.0 | 19.5 | ||
| HPV 18 | 73.9 | 19.4 | 6.7 | 38.647 | <.001 | |
| Mix | 67.5 | 17.5 | 14.9 | |||
| HPV other | 69.8 | 20.2 | 10.0 | |||
DISCUSSION
Our large-scale study of 2895 patients with smear results for NILM, ASC-US and LSIL shows that ECC are equally diagnostic as tools for identifying CIN in HPV positive women with these cytology results. ECC has long been a controversial procedure, with no clear consensus on when to perform it in relation to the colposcopy, with normal cytological results or low-grade cytological abnormalities.7–10 The American Society for Colposcopy and Cervical Pathology (ASCCP) 2012 guideline recommends ECC for HPV-positive patients with ASC-US and LSIL cytology if the colposcopic impression is normal.11 However, the 2017 colposcopy standards suggest reevaluating the indications for and performance of endocervical sampling because of gaps in the evidence.12 The identification of CIN2+ through ECC in cases where the ectocervical biopsy is negative or LSIL is a paramount indicator of the necessity for ECC. In Yousefi et al's cohort study with a small sample size, 15.8% of cases with negative exocervical pathology had a positive ECC test result.13 Among those with a satisfactory colposcopy, 28.3% had positive ECC results. Based on these findings, the authors recommended performing ECC in all patients, regardless of whether the colposcopy is satisfactory or unsatisfactory. Van der Marel et al conducted a study involving 126 patients, where they found the CIN2+ yield of ECC in addition to biopsies to be 11.9%.14 Liu et al reported that among 204 women with ASC-US or LSIL cytology, those with an unsatisfactory examination had a 13% CIN2 or worse yield on ECC (95% CI 6.1-25.7); conversely, when colposcopic examination was normal or satisfactory with visible abnormal lesions, ECC detected less than 5% CIN2 or worse in the endocervix.15 In the study of 555 patients, 333 (60%) had CIN2+ on colposcopy or excision.16 In this study, 48 cases (14.4%) were diagnosed with CIN2+ using ECC alone. Nakamura et al found that ECC increased the diagnostic yield of CIN2+ lesions otherwise missed by colposcopy-guided biopsies alone, with an increase of 2.4%.17
In our study, we found that among patients with normal cervical biopsy results, 1.7% had HSIL. Among patients with LSIL cervical biopsy results, 5% of patients had HSIL in their ECC results for a 6.7% additional yield of CIN2+ from ECC. These findings demonstrate that if ECC had not been performed, the diagnosis of CIN2+ would have been missed in these patients.
We found that ECC is an equally important tool for identifying CIN in HPV-positive women with NILM, not only ASC-US, and LSIL cytology results. We found no statistically significant differences in detection rates of CIN in ECC among the three groups with smear results for NILM, ASC-US, and LSIL. Particularly, the elevation in HSIL rates to a specific extent (12.1%, 13.7%, and 14.7%) underscores the importance of performing ECC not only in patients with ASC-US and LSIL but also in those with NILM who undergo colposcopy. This finding remained consistent in both the normal and abnormal colposcopy groups, with no difference in the rates of CIN detection in ECC among cases with smear results of NILM, ASC-US, and LSIL. This indicates that ECC holds equal importance in diagnosing CIN in all three groups, regardless of the colposcopic appearance.
However, in further analyses, we found that HPV16 positive patients are 2.2 times more likely to have HSIL in ECC. In Massad's study (Guidelines for Endocervical Curettage at Colposcopy),5 it is recommended that ECC be performed in all patients who undergo colposcopy and have a known positive test for HPV types 16 or 18.5 This recommendation is classified as level BIII. The rationale behind this recommendation is that HPV type 16 alone is responsible for more than half of all cervical cancers. Consequently, patients with HPV16 should be given special consideration due to the aggressive nature of their infections. As mentioned, we also found a higher rate of HSIL in patients with HPV16. In our opinion, the likelihood of detecting HSIL in ECC is higher in patients with ASC-US and LSIL smear results, irrespective of HPV type. However, attributing the elevated rate of HSIL in patients with normal smear results to HPV16 positivity, as indicated by our analysis, seems more pertinent. Therefore, we also concluded that regardless of the colposcopic findings, ECC should be performed in all patients who are HPV16 positive with a smear result of NILM, as well as in patients with a smear result of ASC-US or LSIL who were positive for any oncogenic type of HPV.
In the present study, it was observed that the incidence of LSIL in ECC was higher in patients aged 50 years and older. Further analysis revealed that women in the age group of 50-59 years were diagnosed with LSIL at a rate 2.3 times higher, while those aged 60 years and older had a rate 2.8 times higher. The presence of HSIL was also 2.2 times more likely in both age groups. Similarly, during the postmenopausal period, there was a 1.9-fold increase in the LSIL diagnosis during ECC and a 1.3-fold increase in the HSIL diagnosis. These findings are consistent with the existing literature, indicating a correlation with the duration of HPV exposure. It is widely recognized in studies examining the relationship between age and ECC that CINs increase after the age of 40 years, highlighting the importance of routine ECC during colposcopy for patients aged 40 years and older.18,19 In Suebthawinkul et al's study, they observed an increased detection rate of ECC for high-grade lesions in women with low-grade cytological abnormalities.18 In their study, this rate was 8.04%. The routine use of ECC during colposcopy for LSIL in young women is a topic of debate. However, the sensitivity of ECC was higher in women aged over 40 years and post-menopausal women. Therefore, they suggested that ECC may be beneficial for older and post-menopausal women. Similarly, in Solomon et al's study involving LSIL patients, they reached the conclusion that ECC's value as an additional diagnostic technique alongside colposcopically directed biopsy is uncertain for younger women.19 However, they stated in women aged 40 years and older, the sensitivity of colposcopic biopsy decreased while the sensitivity of ECC increased. Consequently, ECC was suggested as beneficial for older women undergoing colposcopy with equivocal or mildly abnormal cytology. According to the results of our study, we recommend ECC in patients aged 50 years and older with any smear result or with any oncogenic HPV type.
Our study has a few limitations. First, we could not determine the components of the of HPV types in ‘mixed’ and ‘other’ groups, which prevented us from including more detailed analyses based on HPV types in our discussion. The ‘mixed’ HPV group consisted of various oncogenic types of HPV combined in different combinations including type 16, 18 and other types. Similarly, ‘other’ groups consisted of various oncogenic types of HPV other than type 16 and 18. Another limitation was the lack of clarity regarding the criteria used to perform biopsies on patients with normal colposcopy results.
According to our study's results, we anticipate that increasing the frequency of ECC following colposcopic biopsy could enhance the detection of CIN cases. This anticipated increase in yield is expected to be particularly pronounced in the subgroup characterized by normal smear results, positivity for HPV 16, and normal colposcopic findings.
In conclusion, we recommend performing ECC in patients with a smear result of NILM who are positive for HPV16, in patients with a smear result of ASC-US or LSIL who are positive for any oncogenic type of HPV, regardless of colposcopic findings. We also recommend performing ECC in patients 50 years and older with any result of smear or any oncogenic HPV type regardless of colposcopic findings.
Funding Statement
None.
CONFLICT OF INTEREST:
None.
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