Clinical analysis of cervical cancer in the second and third trimesters of pregnancy

doi:10.21203/rs.3.rs-3794706/v1

Background

To explore the clinical and prognostic characteristics of patients with cervical cancer in late pregnancy, and provide guidance for clinical decision-making for both doctors and patients.

Methods

A retrospective analysis was conducted on the clinical data of 13 cases of cervical cancer in late pregnancy treated in our hospital from 2008 to March 2022.

Results

The average age of the patients was 33.54 ± 4.98 years old, with 5 cases diagnosed in late pregnancy and 8 cases in mid-pregnancy. The main clinical manifestation was vaginal bleeding, and cervical biopsy confirmed the diagnoses after the patients sought medical attention. Among them, 9 patients had HPV16 infection. Eight patients underwent chemotherapy during pregnancy, and all patients underwent cesarean section to end the pregnancy. Twelve patients underwent radical surgery during cesarean section, and 1 patient underwent surgical treatment after chemotherapy 6 weeks after cesarean section. Eventually, 11 patients gave birth, while 2 patients gave up on neonatal rescue. Among them 1 patient has developed VIN I, 1 patient is lost to follow-up, and 11 patients have been cured without recurrence.

Conclusion

HPV16 infection before pregnancy is a high-risk factor for cervical cancer during pregnancy, and vaginal bleeding during pregnancy should be taken seriously. The prognosis is good after treatment of cervical cancer in the second and third trimesters of pregnancy.

late pregnancy

cervical cancer

outcome

Cervical cancer is a common gynecological tumor during pregnancy, accounting for 71.6% of combined gynecological tumors during pregnancy(Beharee, et al.,2019). However, it is still a rare disease. Due to the easily mistaken bleeding symptoms with pregnancy-related bleedings, and the neglect of cervical screening before pregnancy, pregnant women often lack the corresponding gynecological examinations, which leads to easy misdiagnosis. About half of the patients are diagnosed during pregnancy, and the other half are diagnosed postpartum(Smith, et al.,2001). The treatmcooperation, which poses challenges to clinical doctors. The survival rate of cervical cancer combined with pregnancy does not differ from that of cervical cancer outside of pregnancy(Fukushima, et al.,2009). In mid-late pregnancy, it is difficult for pregnant women and their families to give up the fetus, and due to the enlargement of the uterus and swelling of the vaginal wall, lymph node dissection cannot be easily performed, leading doctors and patients to lean toward preserving the fetus. For cervical cancer in mid-late pregnancy with stage IB or above, choosing neoadjuvant chemotherapy can delay the progression of the disease and complete the pregnancy(Nocarová and Ondruš,2020). However, its effectiveness and safety still need more evidence support. There is a lack of evidence whether the prognosis of cervical cancer combined with pregnancy is worse than that outside of pregnancy, and some studies indicate that pregnancy does not adversely affect cervical cancer survival(Mandic, et al.,2020). This article retrospectively analyzes the clinical diagnosis and treatment process, pregnancy outcomes, and tumor outcomes of 13 cases of cervical cancer in mid-late pregnancy in our hospital. It also retrospectively analyzes the current literature on the diagnosis and treatment of cervical cancer combined with pregnancy, aiming to provide clinical doctors with diagnostic and treatment reference.

Patient

2008 to March 2022, the pregnancy data of 13 patients with late-stage cervical cancer in West China Second Hospital of Sichuan University were selected, as shown in Table 1. The age of the 18 patients ranged from 27 to 43 years old, with an average age of 33.54±4.98 years old. Clinical manifestations in 11 cases began with abnormal vaginal bleeding during mid-pregnancy, 1 case had vaginal discharge, and 1 case had abnormal TCT+HPV screening during pregnancy confirmed by biopsy. The earliest diagnosed pregnancy was 17+6 weeks, and the latest was 36+6 weeks. The gestational age of the infants delivered ranged from 26+2 weeks to 37+6 weeks, with a premature rate of 92.3%. The average birth weight of newborns was 2579 g.

Table 1 General information of the patient

Patient number	Age	Gravidity	Clinical presentation	FIGO Stage	Gestational weeks at diagnosis	Gestational weeks at termination	Newborn birth weight
1	33	G7P2+5	irregular vaginal bleeding	IIIC2	34+2	36+4	2950
2	36	G2P1+1	irregular vaginal bleeding	IB2	17+6	36+6	3300
3	43	G5P2+3	yellowish vaginal discharge with foul odor	IB3-IIIC1p？	32+3	34	2300
4	32	G5P2+3	No	IIA1	20	36+4	2910
5	29	G4P2+2	vaginal bleeding	IB1	21+4	34+4	2640
6	37	G8P3+5	irregular vaginal bleeding	IB1	20+3	35+4	2470
7	27	G4P2+2	vaginal bleeding	IB1	30+4	34+3	2330
8	36	G3P1+2	vaginal bleeding during intercourse	IB2	23+1	26+2	Unknown
9	40	G3P2+1	irregular vaginal bleeding	IB2	36+6	37+6	3280
10	36	G2P1+1	vaginal bleeding	IB	25+4	27+3	Unknown
11	29	G4P2+2	vaginal bleeding	IB2	25	29+2	1340
12	27	G1P1	vaginal bleeding	IB2	31	35+5	2250
13	31	G3P2+1	vaginal bleeding	IB2	32+6	36+6	2600

FIGO the international federation of gynecology and obstetrics;

Clinicopathological data

As shown in Table 2, only the third and twelfth patients had no abnormal TCT results in cervical cancer screening before pregnancy, and HPV testing was not performed. The remaining 11 patients did not undergo cervical cancer screening before pregnancy. All 13 cases were diagnosed with cervical cancer during pregnancy. In the fifth case, vaginal bleeding in early pregnancy presented with no abnormal TCT results, and cervical biopsy suggested genital warts. Regular TCT follow-up in 2+ months showed ASCUS, and biopsy confirmed cervical cancer. Seven cases were confirmed directly by abnormal cervical appearance and biopsy. Two cases did not undergo HPV screening, while the remaining 11 cases showed HPV infection, 9 of which were HPV16 positive. Squamous cell carcinoma was the most common type, accounting 11 cases (84.6%), while adenocarcinoma accounted for 2 cases (15.4%). Eight cases had vascular invasion (61.5%), only one case had no cervical stromal invasion, and one case had parametrical invasion. Lymph node metastasis was found in 4 cases (30.77%). Among them, 8 cases were stage I, 1 case was stage II, and 4 cases were stage III. Patient 1 showed cervical enlargement and lymph node enlargement on MRI at the pregnancy week 34+2, and lymph node metastasis was confirmed by lymph node biopsy during cesarean section.

Table 2 Clinicopathological data

patient number	TCT	HPV	Pathological type	Vascular invasion	Depth of cervicalromal invasion	Parametrial invasion	Lymph node metastases	FIGO stage
1	ASCUS	16	LDSCC	+	deep 1/3	+	+	IIIC2p
2	ASCUS	16	LDSCC	+	middle 1/3	-	-	IB2
3	ASCUS	16	LDSCC	+	deep 1/3	-	+	IIIC1p
4	ASCUS	16	LDSCC	-	middle 1/3	-	-	IIA1
5	ASCUS	53	LDSCC	-	superficial 1/3	-	-	IB1
6	colposcopy biopsy	16、51	LDSCC	+	middle 1/3	-	+	IIIC1p
7	cervical biopsy	16	LDSCC	+	more than 1/2	-	-	IB1
8	cervical biopsy	16	genital verrucous squamous cell carcinoma	-	less than 1/2	-	-	IB2
9	cervical biopsy	42/56	LDSCC	+	more than 1/2	-	-	IB2
10	cervical biopsy	16	LDSCC	+	more than 1/2	-	-	IB
11	cervical biopsy	/	well-differentiated mucinous adenocarcinoma	-	-	-	-	IB2
12	normal	16	moderately differentiated intimal adenocarcinoma	-	less than 1/2	-	-	IB2
13	cervical biopsy	/	LDSCC	+	Middle 1/3	-	+	IIIC1p

ASCUS:atypical squamous cells of undetermined significance;LDSCC: low differentiated squamous cell carcinoma.+:positive; -:negative; FIGO:the international federation of gynecology and obstetrics.

The treatment methods and outcomes are presented in Table 3. Twelve patients underwent cesarean section plus radical surgery for cervical cancer at the same time, except for patient 1. All surgeries were performed through cesarean section plus radical hysterectomy and bilateral salpingectomy and pelvic lymph node dissection. Two cases of adenocarcinoma were accompanied by bilateral oophorectomy, while the remaining cases performed bilateral ovarian displacement surgery. Patient 1 underwent cesarean section, followed by adjuvant chemotherapy and radical surgery for cervical cancer 6 weeks after the operation. Eight patients received neoadjuvant chemotherapy during pregnancy, 7 of which used the TP regimen for 3 cycles with a 3-week interval, and 1 used the BVP regimen. After surgery, 6 patients received radiotherapy and chemotherapy, and 2 underwent postoperative chemotherapy. Patient 6 developed intestinal obstruction after surgery but recovered. There were no postoperative complications in the remaining cases. The follow-up time ranged from 21 months to 13 years and 5 months. One patient was lost to follow-up. No recurrence or metastasis occurred in the remaining 12 cases. Patient 9 showed VIN1 during follow-up after surgery. Eleven newborns survived, and no chemotherapy-related complications occurred.

Table 3 Follow-up outcomes

Patient number	NAC during pregnancy	Surgery	Adjuvant therapy	Follow up time（months）	tumor outcome	neonatal outcome
1	NO	CS+RH+ PL(After 46days of CS)	TP+CHT	27	DFS	Alive
2	TP	CS+RH+PL	RT+CHT	40	DFS	Alive
3	NO	CS+RH+PL	RT+CHT	46	DFS	Alive
4	TP	CS+RH+PL	RT+CHT	53	DFS	Alive
5	NO	CS+RH+PL	NO	72	Cure	Alive
6	TP	CS+RH+PL	NO	83	Cure	Alive
7	TP	CS+RH+PL	RT	39	DFS	Alive
8	BVP	CS+RH+PL	CHT	132	Cure	Died
9	NO	CS+RH+PL	RT+CHT	161	VaIN1	Alive
10	NO	CS+RH+PL	RT+CHT	Lost to follow-up	Lost to follow-up	Alive
11	TP(24+4W)	CS+RH+PL	RT+CHT	116	Cure	Died
12	TP	CS+RH+PL	CHT	21	DFS	Alive
13	TP(33W)	CS+RH+PL	RT+CHT	83	Cure	Alive

NO:no treatment; CS:Cesarean; RH:radical hysterectomy; PL:pelvic lymphadenectomy; RT:radiotherapy; CHT:chemotherapy; NAC:neoadjuvant chemotherapy; TP:paclitaxel + platinum； BVP：bleomycin + vincristine + cisplatin; DFS: disease free survival.

The incidence of cervical cancer during pregnancy is not high, with a prevalence of about 1/2000 to 1/10000(Bo, et al.,2021), accounting for about 10% of all malignant tumors during pregnancy(Lu, et al.,2023). The common clinical symptoms of cervical cancer during pregnancy are not significantly different from cervical cancer outside pregnancy, characterized by irregular vaginal bleeding and exudate, which can be easily confused with early miscarriage or preterm labor. In our report of 13 cases, the diagnosis was only confirmed in the late stage of pregnancy, and 10 of the cases had a history of vaginal bleeding in the early stage of pregnancy. Vaginal bleeding during pregnancy is often considered a pregnancy-related complication, especially in early pregnancy, therefore, gynecological examination is easily ignored. At the same time, due to the influence of pregnancy hormones, the results the Papanicolaou test during pregnancy may not be accurate. Vaginal colposcopy is relatively difficult, and cytology and vaginal colposcopy is less effective in diagnosing cervical cancer during pregnancy(Sonoda, et al.,2021). Therefore, gynecological examination is necessary when vaginal bleeding or discharge occurs during pregnancy. The importance of HPV screening is also highlighted, as two cases of cervical cancer screening before pregnancy did not check for HPV and showed no abnormalities on TCT. Cervical evident hyperplasia was found and a biopsy was performed directly. If cervical cancer screening hasn't been done in the past 3 years, it is to undergo TCT and HPV testing with a vaginal colposcopy if necessary(Lu, et al.,2023). Vaginal colposcopy is safe and feasible for pregnant women and is usually recommended during mid-pregnancy to avoid attributing natural miscarriages to colposcopy(Stonehocker,2013).

Our treatment for cervical cancer during pregnancy involved neoadjuvant chemotherapy, which prolonged the pregnancy and resulted in the birth of a healthy newborn with no congenital complications so far. Chemotherapy is contraindicated in early pregnancy, as it may cause miscarriage, fetal death, and fetal malformations. It is prohibite to use chemotherapy within 10 weeks of pregnancy, especially within 14 weeks. Studies have found that early pregnancy chemotherapy is not associated with increased congenital abnormalities, while chemotherapy in mid to late pregnancy is associated with fetal growth restriction, low birth weight, and preterm labor(Mandic, et al.,2020). However, several studies have shown that neoadjuvant chemotherapy in mid to late pregnancy is safe(Sparano, et al.,2008; Zagouri, et al.,2019) and is an effective alternative for achieving fetal survival(Lopez, et al.,2021). Neoadjuvant chemotherapy can control tumor progression, delay the pregnancy week, promote fetal lung maturation, ensure maternal and fetal survival, and prevent lesion transfer during pregnancy(Mandic, et al.,2020; Bernardini, et al.,2022).Therefore, neoadjuvant chemotherapy is safe and effective in pregnant women with cervical cancer.

The treatment for cervical cancer during pregnancy depends on factors such as the stage of the cancer, tumor size, gestational age, pathological type, and the patient's and family's preference for preserving the fetus. Radical surgery for cervical cancer involves removing the uterus, resulting in permanent infertility for the patient. According to the FIGO guidelines, if cervical cancer is diagnosed before 20 weeks of pregnancy, it is recommended to consider terminating the pregnancy for timely treatment. For pregnancies between 20 and 28 weeks, a comprehensive evaluation is needed to determine whether to continue the pregnancy. IGCS and ESGO consensus recommends that for patients who wish to continue the pregnancy and are under 22 weeks, laparoscopic assessment of lymph node status can be performed before making a decision regarding the pregnancy. In our reported cases, only two patients with late-stage cancer chose immediate treatment, resulting in premature delivery and fetal loss. The remaining 11 patients requested a delay in gestational age to preserve the fetus, and they underwent cesarean section and surgical treatment after 34 weeks of pregnancy. All newborns survived, and the patients are currently under regular follow-up. In a retrospective study of 20 patients with cervical cancer during pregnancy, although there were no significant differences in stage compared to the cases reported, the median follow-up time was 68 months. However, two patients in early pregnancy, one in mid-pregnancy and one in late pregnancy died from the tumor metastasis within 13 months after treatment. More patients chose immediate treatment and abandonment of the fetus (Zhang, et al.,2015). For pregnancies with cervical cancer but without the intention to continue the pregnancy, the approach is similar to treating cervical cancer outside pregnancy. For patients who want to preserve the fetus, treatment should be delayed until the second trimester due to the risk of miscarriage and fetal malformation associated with surgery and chemotherapy(Calsteren, et al.,2010; K?Hler, et al.,2015). Non-ionizing radiation imaging, such as ultrasound and MRI, is recommended for assessing the disease status, which is relatively safe for the fetus(Amant, et al.,2019). If the cancer is in an advanced stage, it is recommended to consider terminating the pregnancy and receive definitive treatment. Lymph node involvement is one of the most important prognostic factors. Vercellino performed laparoscopic pelvic lymphadenectomy in 32 patients with stage II cervical cancer in mid-pregnancy and found that the complications and number of lymph nodes removed were similar to those in non-pregnant patients (Vercellino, et al.,2014), indicating the safety and effectiveness of this surgery during the second trimester. Surgery is recommended for stage Ia-Ib1 cervical cancer. For stage Ib2-IIa, NACT may be more suitable, with the primary goal of stabilizing the tumor and preventing further spread (Amant, et al.,2014). The use of taxanes, platinum-based drugs, anthracyclines, and ifosfamide during pregnancy after 14 weeks is relatively safe (Ricci and Rosa,2016; Strulov, et al.,2018). If anthracycline or other drugs with cardiotoxicity are used during pregnancy, newborns should undergo electrocardiographic examination. Hearing should be carefully monitored throughout infancy after exposure to platinum-based drugs(Geijteman, et al.,2014). The timing of terminating the pregnancy mainly depends on fetal maturity, with a recommended interval of at least 3 weeks after the last chemotherapy cycle to avoid maternal-fetal infection and hematological complications(Tineke, et al.,2017). The FIGO guidelines recommend terminating the pregnancy for cervical cancer no later than 34 weeks of gestation (Bhatla, et al.,2021), while the IGCS and ESGO recommend delaying it until 37 weeks.

In our treatment, two pregnancies were terminated before 28 weeks (one family abandoned the rescue of the newborn), two were between 28-34 weeks (one survived, and another family abandoned the rescue), and nine were after 34 weeks (all survived). Vaginal delivery may increase the risk of cervical dilation or tearing, accelerate tumor spread and metastasis, and be associated with a poor prognosis. Therefore, cesarean section may be a preferable delivery method(Gungorduk, et al.,2016). It is recommended to perform cesarean section after 32 weeks of gestation when fetal lung maturity is achieved(Levy, et al.,2020). Currently, the treatment strategy for such patients mainly includes termination of pregnancy, prolonging treatment for pregnant women, and iatrogenic preterm delivery. From our cases, it can be seen that all newborn outcomes were good without any malformations and other complications.

In summary, cervical cancer during pregnancy differs from normal pregnancy and cervical cancer. Currently, there are few reports on late-stage cervical cancer during pregnancy. Based on our retrospective analysis, first, attention should be paid to bleeding symptoms during pregnancy, and pre-pregnancy screening should be emphasized. Second, patients with cervical cancer during pregnancy should be discussed by a multidisciplinary team, including gynecologic oncologists, high-risk pregnancy obstetricians, neonatologists, radiation oncologists, and psychologists, etc., to provide the best treatment plan based on patient's condition. Third, NACT can prolong the duration of pregnancy, slow down the progression of the disease, and normalize the condition of the newborn. After evaluating the fetal maturity, cesarean section can be performed, and elevated prognosis for the mother can be expected with active surgical treatment, which can provide a certain reference for clinicians and patients.

VIN Vaginal intraepithelial neoplasia

TCT Thinprep cytologic test

HPV human papilloma virus

FIGO The international federation of gynecology and obstetrics

CS cesarean section

MRI Magnetic Resonance Imaging

ASCUS Atypical squamous cells of undetermined significance

IGCS Gynecological Cancer Society

ESGO the European Society of Gynecological Oncology

NACT neoadjuvant chemotherapy

Author contributions YC conceived and designed the study. JZ developed the study methodology. LH acquired,analyzed, and interpreted data. QW wrote the original draft of the manuscript, and all authors wrote, reviewed, and/or revised the manuscript.

Funding None

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

Conflict of interest The authors declare no competing interests.

Ethical approval The study was performed in accordance with the ethical standards of the Declaration of Helsinki (1964) and its subsequentamendments. The study protocol involved human participants were approved by the Ethics Committee of West China Second University Hospital, Sichuan University.

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No competing interests reported.

Clinical analysis of cervical cancer in the second and third trimesters of pregnancy

Status:

Version 1

Abstract

Background

Methods

Results

Conclusion

Introduction

Materials and methods

Results

Discussion

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1