Chao Zhao,Mingzhu Li,Hao Deng,Lihui Wei (Department of Obstetrics and Gynecology, Peking University People's Hospital, Beijing 100044, China)
Foundation Item:
National Key R&D Program of China (2021YFC2701202), Beijing Health Science and Technology Achievements and Appropriate Technology Promotion Project (BHTPP2022008), Research and Development Fund of Peking University People's Hospital (RDL2021-04), Research and Development Fund of Peking University People's Hospital (RDL2022-34)
Corresponding author: Wei Lihui
E-mail:[email protected]
Prof. Wei Lihui
Professor of Obstetrics and Gynecology, Peking University People's Hospital
Honorary Director of the Department of Obstetrics and Gynecology, Peking University
Chairman of the Colposcopy and Cervical Pathology Branch of the Chinese Eugenics Science Association
Member of the International Federation of Colposcopy and Cervical Pathology
Member of the American Society of Colposcopy and Cervical Pathology
Deputy Editor-in-Chief of Chinese Journal of Obstetrics and Gynecology
Editor-in-chief of the Chinese Journal of Clinical Obstetrics and Gynecology
She used to be the vice chairman of the Obstetrics and Gynecology Branch of the Chinese Medical Association, the vice chairman of the Gynecologic Oncology Branch of the Chinese Medical Association, the vice president of the Obstetrics and Gynecology Branch of the Chinese Medical Doctor Association, the vice president of the Chinese Women Physicians Association, the vice president of the Beijing Branch of the Chinese Medical Association, and the chairman of the Obstetrics and Gynecology Branch.
He has won a number of first, second and third prizes of science and technology from the Ministry of Education, Chinese Medical Association, Chinese Society of Prevention, Beijing Municipality, etc., and the Chinese Physician Award.
【Abstract】Cervical cancer is a common female malignant tumor, and its main cause is persistent infection of high-risk human papilloma virus (HPV), which can be effectively prevented, controlled and finally eliminated through tertiary prevention measures such as HPV vaccination for young women, cervical cancer screening in women of appropriate age, and timely treatment of cervical cancer and precancerous lesions. However, there are still many problems in the prevention and treatment of cervical cancer, including the need to further promote the vaccination of women of appropriate age with HPV vaccine, expand the coverage of cervical cancer screening, and choose the treatment of cervical cancer. The purpose of this article is to summarize the current status and existing problems of cervical cancer prevention and treatment in 2023.
【Keywords】cervical cancer, human papillomavirus vaccine, screening, cervical cancer treatment
In March 2023, the National Cancer Center released the prevalence data of malignant tumors in China in 2016 based on the 2016 malignant tumor registration data (as of August 31, 2019) reported to the National Cancer Registry by various cancer registries across the country, among which the number of new cases of cervical cancer continued to increase, reaching 119,300, ranking sixth among new cases of female malignant tumors, and 37,200 deaths, ranking eighth among female malignant tumor deaths, accounting for 18% and 17% of cervical cancer in the world, respectively [1]. ]。 Among women aged 15~44 years in mainland China, cervical cancer ranks third among female malignant tumors in terms of both new cases and deaths, which seriously threatens the life safety of women in mainland China [2].
In November 2020, the World Health Organization (WHO) released the Global Strategy to Accelerate the Elimination of Cervical Cancer [3], proposing that the world should achieve the "90-70-90" stage goal by 2030, that is, 90% of women should be vaccinated against human papilloma virus (HPV) before the age of 15, and 70% of women should be at least 35. At the age of 45, they received one standardized screening, and 90% of patients diagnosed with cervical disease were treated. On the road to cervical cancer prevention and control, the mainland has also carried out a series of actions to accelerate the implementation of the strategy. In particular, in January 2023, China's National Health Commission and 10 ministries and commissions jointly issued the Action Plan for Accelerating the Elimination of Cervical Cancer (2023-2030)[4], which puts forward the main goals of the mainland in eliminating cervical cancer in 2025 and 2030: by 2025, the HPV vaccination service for school-age girls will be promoted on a pilot basis, and the cervical cancer screening rate of school-age women will reach 50%, and the treatment rate of patients with cervical cancer and precancerous lesions will reach 90%; By 2030, we will continue to promote the pilot work of HPV vaccination for school-age girls, and the screening rate of cervical cancer among women of appropriate age will reach 70%, and the treatment rate of patients with cervical cancer and precancerous lesions will reach 90%. The release of the above documents has greatly promoted the prevention and treatment of cervical cancer in mainland China. The purpose of this article is to summarize the progress and existing problems in the field of cervical cancer prevention and treatment in 2023.
1. Promote HPV vaccination for women of appropriate age
At present, the HPV vaccine is a non-immunization program vaccine (category 2 vaccine) in the mainland. In accordance with the provisions of the vaccine instructions and the principle of "informed consent and voluntary self-payment", the vaccination unit should scientifically inform the family members or recipients and provide timely vaccination for the recipients [5-6]. In order to promote HPV vaccination for school-age girls, a lot of publicity, education and promotion work has been done across the country. In 2021, national health cities (districts) will carry out pilot work on innovative models, strengthen health education, and promote HPV vaccination among adolescent girls. Over the past two years, local governments in many provinces, municipalities, autonomous regions, and municipalities directly under the Central Government have actively promoted the vaccination of girls under the age of 15 and formulated vaccination programs based on their respective economic development conditions [7]. At present, the vaccination rate of 13~14-year-old girls in some places (such as Chengdu) has reached 90% [8]. If the HPV vaccination rate of girls in this age group can reach more than 70%, it will definitely reduce the incidence of cervical cancer.
How to promote universal vaccination coverage still needs to be coordinated by multiple parties under the leadership of the government. There are two peak periods of high-risk HPV infection in mainland women: the first peak is 17~24 years old, and the second peak is 40~44 years old [9], and the single infection of high-risk HPV is the main [10], so it is also beneficial for adult women to be vaccinated. With the continuous improvement and quality improvement of vaccine supply chain services in mainland China, more and more women, especially young women, will take the initiative to complete HPV vaccination.
2. Progress and existing problems in cervical cancer screening
Since 2009, when cervical cancer was included in the mainland's "Two Cancer Screening" program, the country has begun to carry out cervical cancer screening for rural women, and has made remarkable achievements in the past 10 years, and has done a lot of exploration in screening methods. This year, seven associations in mainland China jointly issued the Guidelines for Cervical Cancer Screening in China (1) [11], which clarified the purpose of cervical cancer screening in mainland China, formulated cervical cancer screening methods suitable for China's national conditions, recommended high-risk HPV nucleic acid detection as the preferred method for primary screening, and recommended the use of HPV nucleic acid detection methods and reagents that have been recognized by domestic and foreign authorities and clinically proven to be used for primary screening. The Blue Book on the Tertiary Standardized Prevention and Treatment of Cervical Cancer in China [12] and the Guidelines for the Comprehensive Prevention and Control of Cervical Cancer (2nd Edition) [13] also put forward the method of using HPV detection as the primary screening for cervical cancer. At present, the State Food and Drug Administration has successively approved HPV kits for primary screening and combined screening of cervical cancer, as well as a triage method for those who are positive for screening. In 2021, the World Health Organization (WHO) Guidelines for the Screening and Treatment of Precancerous Cervical Lesions (2nd Edition) [13] issued by the World Health Organization (WHO) proposed that DNA methylation detection is a new technology that can be used for cervical cancer screening in the future, providing a new way for abnormal triage of cervical cancer screening. In addition, methods for detecting cervical cancer susceptibility genes are also being studied.
How to expand the coverage of screening is the main problem in cervical cancer screening. In order to expand the coverage of screening, female self-sampling HPV testing is also a new screening method to improve the screening rate of cervical cancer. The World Health Organization (WHO) has included this method as one of the key elements of the screening method [14]. At present, how to use the Internet to do a good job of self-sampling HPV nucleic acid detection mode under the existing situation in mainland China needs to be further explored.
3. Treatment of cervical cancer
3.1 Surgical treatment of cervical precancerous lesions and cervical cancer is problematic
3.1.1 Surgical selection Cervical conization (referred to as cervical conization) is generally divided into two methods: loop electrosurgical excision procedure (LEEP) and cold-knife conization (CKC). Studies have shown that LEEP and CKC are equally effective in the treatment of high-grade squamous intraepithelial lesions (HSIL) [15]. The 2023 and 2024 National Comprehensive Cancer Network (NCCN) guidelines standardize two surgical procedures and update them based on available clinical trial data, including conservative surgical criteria and recommendations for conservative surgery for low-risk, early-stage cervical cancer [16-18].
LEEP has become the "gold standard" for the treatment of HSIL and is now commonly used in clinical practice. However, LEEP has the following problems: (1) If there is a suspicion of microinvasive cancer, the resection range may be insufficient, and the lesion may remain. At present, the 2023 NCCN guidelines have changed the negative margins from at least 3 mm to 1 mm for microinvasive carcinoma, so it is not difficult to meet the standard of 1 mm for negative margins < LEEP. (2) The concept that LEEP requires "whole block excision" is easily ignored in clinical practice. Some doctors mostly perform LEEP by block resection or fragment resection, which affects the interpretation of pathological results. Excluding the technical reasons of the instrument and the operator, the most common reason is that the patient is uncomfortable and unable to fix the position due to incomplete local block anesthesia during the surgical operation, so the NCCN recommends the use of intravenous anesthesia when performing LEEP. However, local anesthesia is still used to complete surgery in mainland China.
CKC is the preferred method for the treatment or diagnostic removal of minimally invasive cancer of the cervix. Stage I.A cervical cancer needs to be diagnosed and determined by cervical conization pathological examination, so as to facilitate the selection of appropriate treatment. When the pathology of the colposcopic cervical biopsy is HSIL and invasive cancer cannot be ruled out, the pathologic diagnosis obtained with CKC may be more reliable, especially to determine whether the margins are cut and whether there is lymphovascular space invasion (LVSI). CKC requires the removal and labeling of the diseased portion and cervical canal tissue in its entirety to provide the pathologist with a complete, non-fragmented sample without electrical damage that facilitates the assessment of marginal status. The cone resection margin is required to have a negative distance of at least 1 mm (negative resection margin means that there is no invasive lesion or high-grade squamous intraepithelial lesion at the resection margin), and the resection depth is at least 10 mm, which can be increased to 18~20 mm in childbearing patients. LEEP can also be used if the lump can be excised in its entirety and sufficient negative margins can be achieved, but the impact of the cauterized margins on the pathologic judgment should be minimized. In addition, it is acceptable if LEEP can ensure sufficient margins and properly marked. In addition to pregnancy, cervical conization should be accompanied by endocervical curet-tage (ECC).
3.1.2 Impact of LVSI on treatment decisions for cervical cancer Although LVSI does not affect staging, it determines the treatment strategy for whether it is positive or not. Szala et al. [19] suggested that LVSI is the basis for tumor metastasis by allowing tumor thrombus to spread through blood vessels. LVSI has been found to be closely related to tissue type, depth of interstitial invasion, tumor volume, parauterine invasion, lymphatic metastases, and survival [20]. Yan et al. [21] conducted a retrospective study on 485 patients with stage I.B~II.A cervical cancer of the Federation International of Gynecology and Obstetrics (FIGO), and the results showed that the incidence of LVSI was significantly correlated with FIGO stage (P=0.008), interstitial invasion depth (P=0.001), There was a significant correlation between positive lymph node metastasis (P=0.001), and the overall survival (OS) rate of patients in the LVSI group was significantly lower than that in the non-LVSI group (9.2%vs. 2.1%, P=0.009) after 28~55 months of follow-up. All of the above studies have shown that LVSI is an important prognostic factor for cervical cancer patients.
Studies have shown that the rate of lymphatic metastasis is < 1 percent in patients with cervical cancer stage I.A1 and no LVSI after cervical conization [22]. Further treatment is carried out by the following methods [17]:(1) The pathology report of the resected specimen is negative, and there is a negative distance of at least 1 mm, and those with contraindications to surgery are recommended to be followed up for observation after surgery. (2) For patients without surgical contraindications, modified radical cervical cancer resection is recommended. (3) For patients with positive margins after cervical conization, it is recommended to revert to cervical conization, and the depth of infiltration is evaluated to exclude stage I.A2 and I.B1. If cervical conization is not performed and direct surgery is performed, modified radical cervical cancer resection is recommended for HSIL margins, and modified radical hysterectomy + pelvic lymphadenectomy or sentinel lymph node imaging is recommended for patients with cancer margins. (4) Brachytherapy ± pelvic external beam radiation therapy are recommended for patients with positive conone resection margins (HSIL or cancer) and contraindications to surgery. In addition, several issues should be paid attention to when performing cervical conization: (1) ECC should be added to those with indications, (2) due to the low incidence of ovarian metastasis in early squamous cell carcinoma, premenopausal patients < 45 years old can choose to preserve the ovaries, and (3) the detection rate and accuracy of tumor diameter < 2 cm are the highest during sentinel lymph node imaging.
3.1.3 Fertility-preserving decision-making for early-stage cervical cancer Patients with stage I.A2~I.B1 cervical cancer diagnosed by cervical conization need to meet ConCerv criteria (enrollment criteria) [16]:(1) no LVSI, (2) negative margins, (3) squamous cell carcinoma (any grade) or common type adenocarcinoma (G1 or G2), ;(4) tumor diameter≤2 cm, (5) depth of invasion ≤10 mm, (6) no metastasis at other sites on imaging examination. In principle, it is recommended for patients with stage I.B1 and elective stage I.B2 for cervical cancer with fertility preservation, and radical trachelectomy can be performed vaginally or transabdominal for patients with tumor diameters of ≤2 cm. Stage I.B1 and elective stage I.B2 that do not meet all ConCerv criteria should undergo radical trachelectomy + pelvic lymphadenectomy ± para-aortic lymph node resection, and sentinel lymph node imaging may be considered. It is up to the patient and physician to decide whether to remove the uterus after childbirth, but it is recommended that the uterus be removed after the patient has completed childbirth if the fluid-based cytology continues to be abnormal or the HPV test is persistently positive. In addition, due to lack of evidence, fertility preservation is not recommended for patients with small cell neuroendocrine tumors and gastric adenocarcinoma. If there is no fertility desire, total extrafascial hysterectomy + pelvic lymph node resection (or sentinel lymph node development) can be performed.
The presence or absence of LVSI and the preservation of fertility requirements should be approached differently [16]. The following methods can be selected for stage I.A1 with LVSI and stage I.A2 and fertility preservation: (1) radical trachelectomy + pelvic lymph node resection, sentinel lymph node scintigraphy can be considered; (2) cervical conization + pelvic lymph node resection, sentinel lymph node scintigraphy can be considered; (3) postoperative follow-up observation for patients with negative conone margins of at least 1 mm; (4) conization of patients with positive margins can be repeated with negative margins of at least 1 mm or trachelectomy. For stage I.A1~I.A2 with LVSI without fertility retention, the following methods can also be selected: (1) modified radical hysterectomy + pelvic lymphadenectomy, sentinel lymph node imaging can be considered; (2) patients with surgical contraindications or refusal of surgery can be treated with brachytherapy± and pelvic external beam radiation therapy, and I.A2 stage with LVSI can be considered with cisplatin (can not tolerate cisplatin with carboplatin) monotherapy concurrent radiotherapy.
3.1.4 Controversy over laparoscopic cervical cancer surgery The 2015-2019 NCCN guidelines and the 2018 FIGO report recommended indications for laparoscopic cervical cancer surgery in the cervical cancer surgery pathway. However, the results of a prospective multicenter randomized controlled trial, LACC-RCT [23], published in 2018 and a retrospective cohort study [24], overturned the perception that laparoscopic surgery is feasible for cervical cancer, and clearly proposed that laparotomy is the mainstream surgical approach for cervical cancer, but did not negate the laparoscopic surgical approach for specific patients. Whether laparoscopic surgery can be performed for cervical cancer is the focus of controversy on the choice of indication. Since 2019, the NCCN has recommended open surgery for patients with cervical cancer, and laparoscopic surgery is no longer recommended [25].
Experts from mainland China have proposed the advantages of laparoscopic surgery for early-stage cervical cancer, and proposed that the principle of tumor-free surgery should be strictly followed during surgery [26]. A number of retrospective studies at home and abroad have also shown that patients with cervical cancer with a tumor diameter of <2 cm can undergo minimally invasive surgery and the prognosis is not inferior to laparotomy, and further analysis suggests that the reason for the poor prognosis caused by laparoscopy is most likely due to insufficient tumor-free measures during surgery, mainly including the use of uterine manipulators and improper vaginal incision [27-31]. Because the squeezing of cervical cancer tissue by the uterine manipulator causes the tumor cells to fall off, vaginotomy increases the chance of tumor cells spreading in the pelvis, which in turn promotes the recurrence and metastasis of the tumor. In a large retrospective study from various European countries, the use of uterine manipulators significantly increased the risk of recurrence in patients with early-stage cervical cancer (HR=2.76). The study also analyzed the role of protective vaginal closure (proximal vaginal closure and distal closure of the vagina prior to vaginotomy) in minimally invasive surgery, and the results showed that protective vaginal closure can significantly reduce the recurrence rate, and it is recommended to perform protective vaginal closure during minimally invasive surgery. In 2023, the Guidelines for the Diagnosis and Treatment of Cervical Cancer formulated in mainland China standardize the management strategies of laparoscopic cervical cancer surgery, and combined with multiple meta-analyses, it is proposed that laparoscopic surgery for cervical cancer should be carefully selected under the premise of full knowledge and explicit consent of patients [32].
3.2 Principles for selecting postoperative adjuvant therapy according to the risk factors for cervical cancer
Any one of the risk factors for cervical cancer, including positive nodes, positive margins, and parauterine invasion, is recommended for further imaging to identify metastases at other sites, followed by supplemental external pelvic radiation therapy + concurrent platinum-based chemotherapy ± brachytherapy [16].
Intermediate-risk factors (tumor size, interstitial invasion, positive lymphatic vasculature) for cervical cancer supplemented with external pelvic radiation therapy ± platinum-containing concomitant chemotherapy according to the Sedelis criteria [32]. The Sedelis criteria are primarily used in squamous cell carcinoma, and histological-specific nomograms of squamous cell carcinoma and adenocarcinoma may provide new tools to model recurrence risk and recommend adjuvant therapy. Depth of invasion is an important risk factor for recurrence of squamous cell carcinoma, and tumor size is an important risk factor for adenocarcinoma recurrence, and this risk increases with positive LVSI (Table 1). However, intermediate-risk factors are not limited to the Sedelis criteria, such as adenocarcinoma and tumor proximity to the resection margin [16].
Low-risk factors for cervical cancer meet the ConCerv criteria [16]. Stage I.B1, I.B2, and II.A1 who do not meet all ConCerv criteria can choose the following methods: (1) radical hysterectomy + pelvic lymphadenectomy ± para-aortic lymph node resection, sentinel lymph node imaging may be considered; (2) pelvic external beam radiation therapy (± concurrent cisplatin monotherapy chemotherapy at the same time, carboplatin for those who cannot tolerate cisplatin) + brachytherapy. Patients who do not choose surgery for stage I.B3 and II.A2 can choose the following methods: (1) pelvic external beam radiation therapy + platinum-containing concurrent chemotherapy + brachytherapy, (2) radical hysterectomy + pelvic lymph node resection ± para-aortic lymph node resection, (3) pelvic external radiation therapy + platinum-containing concurrent chemotherapy + brachytherapy + hysterectomy (suitable for poor radiotherapy effect and cervical lesions that are too large to be covered by brachytherapy).
3.3 Treatment of advanced cervical cancer
Most cases of advanced cervical cancer ≥stage II.B) are treated with concurrent chemoradiotherapy. Radical hysterectomy or radical hysterectomy followed by neoadjuvant chemotherapy may be preferred in some mainland II.B cases. Pelvic organ dissection is still possible for patients with central pelvic recurrence or persistent lesions after radiation therapy [33]. Before surgery, it is necessary to determine whether there is distant metastases, if the recurrence is confined to the pelvis, surgical exploration can be performed, and pelvic organs can be removed if the pelvic wall and lymph nodes are not invaded. Depending on the location of the tumor, anterior, posterior, or total pelvic organ excision is used.
In 2023, many new recommendations were also put forward internationally for systemic chemotherapy and immunotherapy for cervical cancer [34]. The Chinese Expert Consensus on Immunotherapy for Gynecologic Malignancies (2023 Edition) issued by the Tumor Endocrinology Committee of the Chinese Anti-Cancer Association recommends five immunosuppressants for the treatment of recurrent and metastatic cervical cancer that have failed prior therapy [35].
4. Summary
At present, a complete level 1, 2 and 3 prevention and treatment system has been established for the prevention and treatment of cervical cancer. Because the cause is clear, there is a prophylactic HPV vaccine that targets the cause. Mature cervical cancer screening and diagnosis methods and standardized treatment strategies from precancerous lesions to cervical cancer have made cervical cancer the first cancer to be eliminated in human beings. Under the leadership of the government, the mainland has worked with various parties, continuously explored, and developed a cervical cancer prevention and treatment strategy suitable for the mainland's national conditions, so that the prevention and treatment of cervical cancer will continue to move forward. In November 2023, at the 18th International Federation for Cervical Pathology and Colposcopy (IFCPC) Congress, China won the right to host the 20th IFCPC in 2029. It is expected that at the international conference in 2029, China will show the world the achievements made by the mainland on the road to eliminating cervical cancer in combination with the strategic goal of global elimination of cervical cancer proposed by the WHO.
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