Focused Ultrasound versus the Loop Electrosurgical Excision Procedure to Treat Women with Cervical High-grade Squamous Intraepithelial Lesions Under 40: A Retrospective Study

doi:10.21203/rs.3.rs-3238882/v1

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Research Article

Focused Ultrasound versus the Loop Electrosurgical Excision Procedure to Treat Women with Cervical High-grade Squamous Intraepithelial Lesions Under 40: A Retrospective Study

https://doi.org/10.21203/rs.3.rs-3238882/v1

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published 03 Feb, 2024

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Background

To evaluate whether focused ultrasound (FUS) or the loop electrosurgical excision procedure (LEEP) is a more feasible treatment for cervical high-grade squamous intraepithelial lesions (HSILs) among women of reproductive age.

Methods

Retrospective case record review of patients under 40 years treated for cervical HSIL using either FUS or LEEP from 1 September 2020 to 31 May 2022. Patients were followed up for cure, recurrence, human papillomavirus (HPV) clearance, and complications within 1 year following treatment. Odds ratios and 95% confidence intervals for no evidence of disease or HPV clearance associated with the treatment modalities and other covariates were estimated using univariate and multivariate logistic regression models.

Results

Among 1054 women who underwent FUS or LEEP, 225 met our selection criteria, of which 101 and 124 received FUS and LEEP, respectively. No significant difference was found in the cure rate during the 3–6-months follow-up (89.11% vs. 94.35%, P = 0.085), nor was there any such difference in the recurrence rate during the 6–12-months follow-up (2.22% vs. 1.71%, P = 0.790) between the two therapies. Both groups showed increasing cumulative HPV clearance rates over time without statistically significant differences (74.23% vs. 82.79%; P = 0.122, during the 3–6-months follow-up, and 84.95% vs. 89.17%; P = 0.359, during the 6–12-months follow-up). Furthermore, the incidence of complications caused by the two techniques was found to be similar. (5.0% vs. 5.6%, P = 0.818).

Conclusion

We found a similarity in effectiveness, safety and reliability between FUS and LEEP in treating women with HSIL under 40.

Focused ultrasound

Loop electrosurgical excision procedure

High-grade squamous intraepithelial lesions

HPV

Efficacy

Cervical cancer-related mortality is a public health concern for women, especially those living in low- and middle-income countries (LMICs) [1]. This cancer has a prolonged precancerous phase known as high-grade squamous intraepithelial lesions (HSILs). Persistent high-risk human papillomavirus (HPV) infection is the primary cause of these precancers and cancers [2]. Therefore, cervical cancer can be effectively prevented through high quality screening and timely treatment of HSIL [3].

Treatment options for HSIL can be categorized as excision and ablation. Cervical conization, which includes cold knife conization and the loop electrosurgical excision procedure (LEEP), is the current preferred treatment method. As an outpatient procedure, LEEP is already the first choice in high-resource settings because it has high efficacy and can provide a tissue specimen for pathologic examination [4]. Excisional methods are widely used; however, it does seem clear that excision is associated with an increasing risk of adverse reproductive outcomes, including preterm delivery and perinatal mortality [5, 6].

Due to the lower technical requirements, ablation is simpler than LEEP and usually involves cryotherapy, laser ablation, and thermal ablation. Furthermore, compared with excisional techniques, previous studies have shown that there is no overwhelming superior technique for eradicating HSIL [7, 8]. Meanwhile, women who underwent ablative therapy were not at increased risk of preterm delivery (regarding births that occurred after the procedure) [5, 6]. With the concern of increasing the likelihood of cervical incompetence, women of reproductive age with plans for future conception prefer ablation as a treatment modality.

As a new ablative technique, focused ultrasound (FUS) is eco-friendly and noninvasive. Published studies have confirm the high clinical efficacy of FUS in the treatment of chronic cervicitis and cervical lesions [9–13]. A previous study by Qin Y demonstrated that, compared to LEEP, FUS had a higher HPV elimination rate in HPV-related HSIL women aged under 30 [9]; however, it did not evaluate the therapeutic efficacy and safety. In addition, due to the late marriage, late childbearing, and three-child policies in China, there are more and more women aged over 30 with plans for future conception. Therefore, the application of this technique to HSIL patients of reproductive age requires more investigation.

By evaluating and comparing the efficacy and safety of the two treatments, this study aims to provide evidence-based recommendations for the optimal management of HSIL in women of reproductive age.

This study involved a retrospective cohort design of FUS vs. LEEP treatment among women (< 40 years old) with biopsy-confirmed HSIL at the Second Affiliated Hospital of Chongqing Medical University between 1 September 2020 to 31 May 2022. As the same hospital administrative database was used for our previous study on the comparison of FUS and cryotherapy [11], the partially overlapping retrieval time resulted in a portion of patients who participated in both the studies. All patients were given informed consent to review their medical records according to the ethical approval guidelines (Ethics Research Committee of the hospital reference NO. 201938).

Data were obtained from the records if the following criteria were met: patients aged 21–40 years with biopsy-proven HSIL were treated using either FUS or LEEP; colposcopic examinations were satisfactory (complete visualization of the squamocolumnar junctions and the entire lesions); lesions neither involved more than 75% of the ectocervix nor did it extend to the endocervix or vagina; findings on endocervical curettage were negative; no evidence of underlying cancer or glandular epithelial lesions was found; by 31 May 2023, patients with complete data had been followed up for 3–6 months and 6–12 months. The exclusion criteria for patients in this study were as follows: (1) pregnancy, (2) previous ablative or excisional treatment for cervical HSIL, (3) current gynecological infection, and (4) significant medical illness that may place patients at medical risk.

FUS ablation was done using the Model-CZF300 ultrasonic therapeutic apparatus for Gynecology under the colposcopic guidance, as described in our previous study [11]. The device was developed by Chongqing Haifu Medical Technology Co., Ltd. (Chongqing, China). The treatment probe covered with a coupling gel was applied over the transformation zone and lesions with 2–5 mm/s velocity for approximately 3–5 min until the surface of the cervix shrunk.

LEEP was carried out using the DGD-300B-2 electrosurgical apparatus (Beilin Electronics Co., Ltd., Beijing, China) under local anaesthesia. Following standard practice, resection was performed under the colposcopic guidance using loop electrodes of appropriate diameter according to the type of transformation zone and the extent of lesions. Hemostasis was achieved by electrocoagulation using a ball electrode.

Postprocedure care instructions were given to the patients. All patients were counseled to abstain from tampons, vaginal douching, and sexual intercourse for at least 4 weeks. Furthermore, providers discussed the precautions and situations for seeking medical advice, including heavy vaginal bleeding, foul-smelling or pus-like discharge, fever for > 2 days, or severe lower abdominal pain.

All patients were advised to return for follow-up examinations at 3–6 months and 6–12 months after FUS or LEEP treatment. Cotesting with thin-layer liquid-based cytology technology (TCT), HPV typing test, and colposcopy were performed at each visit. If one of the tests was abnormal, any identified abnormal areas or endocervical sampling was recommended. A follow-up appointment was scheduled to review the pathology and plan for further evaluation as per guidelines.

The primary post hoc outcome was the efficacy of the two treatment methods, including no evidence of disease, HPV clearance, and recurrence. Irrespective of the HPV clearance, the criteria for defining "no evidence of disease" during the follow-up period ranged from negative screening results for cytology and colposcopy to histological confirmation of the absence of disease if a biopsy sample was obtained. HPV clearance would be identified during the follow-up period as the absence of the same specific HPV type that was detected at baseline. Recurrence was defined as a subsequent biopsy result of HSIL or higher during the 6–12-months follow-up in patients who were considered disease free at the first follow-up. As an additional post hoc outcome, the safety of the two treatments was evaluated by assessing the number of complications arising from the procedures. Severe pain or cramps requiring medication during or after treatment, vaginal discharge or bleeding requiring a hospital visit, infection requiring antibiotics, and cervical stenosis requiring dilation were considered as complications caused by the procedure.

All data were analyzed via SPSS version 26 (IBM, Armonk, NY, USA). Mann-Whitney U-test was used for continuous variables with a skewed distribution, while Fisher's exact test was utilized for categorical variables. Odds ratios and 95% confidence intervals for no evidence of disease or HPV clearance associated with the treatment modalities and other covariates (age, educational background, contraception, lifetime sexual partners, parity, and HPV status) were estimated using univariate and multivariate logistic regression models. P < 0.05 was considered to be statistically signifificant.

Overall, the hospital records of 1054 patients with cervical diseases treated with FUS or LEEP from 1 September 2020 to 31 May 2022, were searched. A total of 225 patients with histologically proven HSIL met our selection criteria, of which 101 (44.9%) and 124 (55.1%) received FUS and LEEP, respectively. The enrolment profile of this study is shown in Fig. 1.

Table 1 shows the characteristics of the remaining 225 patients. The distributions of age, contraceptive method, total lifetime sexual partners or parity were not balanced between the FUS and LEEP groups. However, the other baseline characteristics were similar. The median age of LEEP patients was higher than that of FUS patients (P = 0.000). Compared with patients treated with LEEP, those treated with FUS preferred to use condoms for contraception (75.25% vs. 58.06%), and were found to have more lifetime sexual partners (P = 0.000) but less parity (P = 0.000).

Table 1

Baseline characteristics by Treatment Group
		FUS(n = 101)	LEEP(n = 124)	U/χ²	P
Age	Median (lower quartile, upper quartile)	26.91(24.00,31.00)	34.25(32.00,37.00)	U = 9.610	0.000
	range	18–38	21–40
Educational background	<University	31(30.69%)	47(37.90%)	1.623	0.203
	≥University	70(69.31%)	77(62.10%)
Contraception	Condom	76(75.25%)	72(58.06%)	11.999	0.002
	Others^*	10(9.90%)	32(25.81%)
	None	15(14.85%)	20(16.13%)
Lifetime sexual partners	1–2	69(68.32%)	106(85.48%)	13.483	0.000
	≥ 3	32(31.68%)	18(14.52%)
Parity	0	73(72.28%)	17(13.71%)	119.226	0.000
	1	26(25.74%)	74(59.68%)
	≥ 2	2(1.98%)	33(26.62%)
HPV status	HPV16/18 infection	50(49.51%)	53(42.74%)	3.435	0.179
	Non-HPV16/18 infection	47(46.53%)	69(55.65%)
	Negative	0(0.00%)	0(0.00%)
	Unknown	4(3.96%)	2(1.61%)
*Others include intrauterine device, contraceptives, subdermal arm implant, tubal ligation and coitus interruptus.

Table 2 revealed that there was no significant difference in the cure rate during the 3–6-months follow-up (89.11% vs. 94.35%, P = 0.085) or in the recurrence rate during the 6–12-months follow-up (2.22% vs. 1.71%, P = 0.790) between the two therapies. Furthermore, both groups showed increasing cumulative HPV clearance rates over time without statistically significant differences, 74.23% vs. 82.79% (P = 0.122) during the 3–6-months follow-up and 84.95% vs. 89.17% (P = 0.359) during the 6–12-months follow-up, respectively (Table 2).

Table 2

Efficacy of FUS and LEEP
		FUS	LEEP	χ²	P
3–6 months
	Over all participants followed up	101	124
	no evidence of disease	90(89.11%)	117(94.35%)	2.970	0.085
	HPV-positive at baseline participants followed up	97	122
	clearance of HPV	72(74.23%)	101(82.79%)	2.386	0.122
6–12 months
	No evidence of disease at 3-6month follow-up participants followed up	90	117
	recurrent disease	2(2.22%)	2(1.71%)	0.071	0.790
	HPV-positive at baseline participants followed up	93	120
	clearance of HPV	79(84.95%)	107(89.17%)	0.843	0.359

The effects of various related factors on the cure rate during the 3–6-months follow-up and the HPV clearance rate during the 6–12-months follow-up are shown in Tables 3 and 4, respectively. Per our findings, each patient’s age, educational background, contraception, number of sexual partners, parity, and HPV status did not have any significant association with the cure rate or the HPV clearance rate. After adjustments, FUS and LEEP still had similar cure rates during the 3–6-months follow-up and the HPV clearance rate during the 6–12-months follow-up.

Table 3

Logistic regression analysis for determining patient characteristics associated with cure rates during the 3–6-months follow-up
		Univariate analysis		Multivariate analysis
Variable		OR(95%CI)	P Value	OR(95%CI)	P Value
Treatment	FUS	0.490(0.182–1.313)	0.156	0.407(0.097–1.708)	0.219
	LEEP	1		1
Age		0.995(0.907–1.093)	0.921	0.867(0.749–1.003)	0.055
Educational background	<University	1.067(0.384–2.961)	0.901	1.040(0.345–3.137)	0.944
	≥University	1		1
Contraception	Condom	0.282(0.036–2.216)	0.229	0.293(0.036–2.415)	0.254
	Others	0.382(0.038–3.850)	0.415	0.316(0.030–3.373)	0.340
	None	1		1
Lifetime sexual partners	1–2	1.000(1.000−3.185)	1.000	0.746(0.210–2.654)	0.651
	≥ 3	1		1
Parity	0	0.435(0.091–2.072)	0.296	0.301(0.043–2.125)	0.228
	1	1.152(0.213–6.222)	0.870	1.196(0.203–7.051)	0.843
	≥ 2	1		1
HPV status	HPV16/18 infection	2.089(0.219–19.885)	0.522	1.548(0.145–16.473)	0.717
	Non-HPV16/18 infection	2.700(0.281–25.977)	0.390	2.312(0.210−25.434)	0.493
	Negative^*	-	-	-	-
	Unknown	1		1
*There was no HPV-negative patient.

Table 4

Logistic regression analysis for determining patient characteristics associated with HPV clearance rates during the 6–12-months follow-up
		Univariate analysis		Multivariate analysis
Variable		OR(95%CI)	P Value	OR(95%CI)	P Value
Treatment	FUS	0.644(0.290–1.428)	0.279	1.561(0.487–5.004)	0.454
	LEEP	1		1
Age		0.944(0.874–1.021)	0.148	1.032(0.915–1.165)	0.607
Educational background	<University	1.672(0.676–4.135)	0.266	1.318(0.507–3.424)	0.571
	≥University	1		1
Contraception	Condom	0.710(0.228–2.210)	0.554	0.840(0.253–2.791)	0.776
	Others	2.452(0.421–14.284)	0.319	2.129(0.346–13.086)	0.415
	None	1		1
Lifetime sexual partners	1–2	1.175(0.467–2.952)	0.732	0.793(0.295–2.131)	0.646
	≥ 3	1		1
Parity	0	0.129(0.016–1.009)	0.051	0.122(0.013–1.162)	0.067
	1	0.275(0.034–2.235)	0.227	0.253(0.030–2.134)	0.206
	≥ 2	1		1
HPV status	HPV16/18 infection	2.472(0.249–24.561)	0.440	2.170(0.200−23.520)	0.524
	Non-HPV16/18 infection	1.347(0.142–12.760)	0.795	1.096(0.105–11.440)	0.939
	Negative^*	-	-	-	-
	Unknown	1		1
*There was no HPV-negative patient.

Almost all patients in both groups reported no or minimal discomfort during or immediately after the procedure. Twelve complications related to the procedures were recorded: 5 of 101 (5.0%) in the FUS group and 7 of 124 (5.6%) in the LEEP group (P = 0.818). Among these recorded cases, eight patients experienced heavy postoperative bleeding requiring vaginal gauze packing (FUS, n = 3; vs. LEEP, n = 5); two patients suffered moderate post-operative lower abdominal cramps and required painkillers (FUS, n = 1; vs. LEEP, n = 1); one patient receiving FUS had a localised cervical infection with the need for oral antibiotics; one patient receiving LEEP had a cervical stenosis that required dilation 2 months after the procedure. None of these complications were life-threatening, and none of the patients required hospitalization.

Appropriate management of HSIL is crucial for the success of cervical cancer screening programs to reduce the incidence of cervical cancer. Unfortunately, the screening in LMICs has not been as effective, in part due to inappropriate treatment for women with HSIL. The major challenge is the lack of well-trained medical personnel who are able to perform colposcopy and HSIL treatment in primary healthcare facilities [14, 15]. Removal of HSIL by LEEP is an effective and safe treatment option, with low recurrence rates and high HPV clearance rates [8]. Nonetheless, compared with ablation, LEEP requires highly skilled medical personnel and an expensive piece of equipment, produces odors and possible viral-laden smoke, and increases the risk of preterm labor in subsequent pregnancies for women of reproductive age.

As a promising therapeutic modality, FUS provides a new noninvasive method to ablate the lesions. From a practical perspective, FUS offers several advantages over conventional treatment methods. Firstly, FUS equipment is relatively cheaper compared to other surgical tools, making it a more cost-effective option for patients and healthcare providers. Additionally, the duration of operative training required to perform FUS procedures is much shorter than traditional treatment methods, meaning that medical professionals can quickly learn the technique and start providing patients with quality care. Finally, FUS offers conformal therapy, which is achieved by moving the probe. Furthermore, previous studies have confirmed that the treatment of HPV-related cervicitis or cervical lesions using FUS is effective, acceptable, and safe [9–13]. By increasing the availability and accessibility of precancer treatment, FUS could be used to treat HSIL patients in low-resource settings, appropriately performed by trained mid-level providers in primary healthcare services.

In this retrospective study, patients in the LEEP group had a higher median age and parity than those in the FUS group, and were less likely to choose condoms for contraception. Therefore, the clinical baseline data showed that younger women with fertility needs would prefer FUS for HSIL when the ablation criteria were met. To ensure the comparability of the FUS and LEEP groups, we analyzed factors that may affect the treatment efficacy and HPV clearance using logistic regression. As a result, both univariate and multivariate logistic regression analysis showed that no relevant factors had significant effects on the cure rate and the HPV clearance rate.

In terms of efficacy, the cure rate and the recurrence rate were similar between the two treatments for HSIL. In our study, the cure rate of LEEP was slightly higher (although the difference was not statistically significant) than that of FUS. In addition, we found that the incidence of disease-free was also higher than that reported in most previous publications [16–19]; however, the recurrence rate of LEEP was similar to that reported in previously published studies [7, 16]. Differences in study methods, follow-up periods and selection criteria may account for this discrepancy. Regarding FUS efficacy, our results showed that FUS was not inferior to LEEP, with a cure rate of 89.11% during the 3–6-months follow-up and a recurrence rate of 2.22% during the 6–12-months follow-up. These results are consistent with findings on effectiveness in similar settings in other publications, such as our previous studies that reported cure rates of 88.90–89.70% [10–11] and a previous study conducted by Zhou H et al. who reported a cure rate of 82.80% [13]. However, in our previous studies, no recurrence was observed in patients with biopsy-proven HSIL receiving FUS. The higher recurrent rates are because of differences in study methods and sample sizes.

As is already known, the main risk factor for the persistence or recurrence of HSIL after treatment is persistent HPV infection [20]. Previous research has shown that the HPV test is highly sensitive, with a negative predictive value of almost 98% for detecting recurrence at 6 months after treatment [21]. This means that women whose HPV results are negative after treatment stand less risk of recurrence [22]. It is noteworthy that our study found no significant difference in HPV negativity rates after either FUS or LEEP (74.23% vs. 82.79% during the 3–6-months follow-up and 84.95% and 89.17% during the 6–12-months follow-up). The HPV clearance rates of FUS were consistent with those reported in our previous studies [10–11] but lower than those reported by Qin Y [9]. The different inclusion criteria based on age, type of transformation zone, HPV status, etc., and the different criteria for clearance could be the reasons why the HPV clearance rate was lower. Consequently, these will need to be considered in future prospective, multicenter large-sample studies. Compared with the clearance of HPV which is in the range of 60–87% within 12 months of treatment from previous studies [23–28], the accumulated clearance rate observed in our study is higher, and it was most possibly caused by differences in regions and age ranges of HSIL patients.

The study found that both FUS and LEEP were safe and well-tolerated procedures for treating women with HSIL. Adverse effects and complications were rare and minor, and there was no significant difference in incidence rates between the two treatments. Patients mainly experienced easily controllable adverse effects or complications such as postoperative bleeding or lower abdominal cramps. This is consistent with previous researches on the safety of the two procedures [10–11, 13, 29]. Thus, the low frequency of adverse events and complications associated with FUS indicate that this new ablation is a highly safe treatment option for HSIL with good acceptability.

The present study was limited by its retrospective design and missing data on some patient characteristics. These limitations may have an impact on the power of the study, however, they are common in clinical practice. Another major limitation was that women with HSIL who underwent FUS or LEEP were followed up for only one year after treatment; therefore, long-term follow-up studies are needed in the future. It is also important to note that the study was conducted at only one hospital and it may not be possible to generalise the results to the entire population. Prospective, randomized controlled trials are required to confirm these results and determine the impact of FUS on fertility.

Our study supports FUS ablation as an effective treatment for HSIL patients of reproductive age due to its low recurrence rate and high HPV clearance rate.

FUS

Focused Ultrasound

HSIL

High-grade Squamous Intraepithelial Lesions

HPV

Human Papillomavirus

LEEP

Loop Electrosurgical Excision Procedure

LMICs

Low- and Middle-income Countries

TCT

Thin-layer Liquid-based Cytology Technology

Acknowledgements

None.

Author contributions

Linlin Xiao was responsible for conceptualization, study design, statistical analysis, and manuscript writing and editing. Shufang Chang contributed to supervision, methodology and investigation. Xu Dong, Jiangchuan Sun, Xuerui Zhang and Qing Feng contributed to data curation and validation. All authors read and approved the final manuscript.

Funding

This work was supported by Chongqing medical scientific research project (Joint project of Chongqing Health Commission and Science and Technology Bureau) [No.2022ZDXM007], Kuanren Talents Program of second affiliated hospital of Chongqing Medical University, Kuanren Innovation Team Program of second affiliated hospital of Chongqing Medical University, Future Medical Youth Innovation team of Chongqing Medical University.

Availability of data and materials

The data that support the findings of this study are not publicly available due to privacy or ethical restrictions, but are available from the corresponding author upon reasonable request.

Ethics approval and consent to participate

This study was approved by the Ethics Research Committee of the Second Affiliated Hospital of Chongqing Medical University (NO. 201938) and performed in accordance with the tenets of the Declaration of Helsinki. The requirement for written informed consent was waived by the Ethics Research Committee because data were anonymized and retrospectively analyzed.

Consent for publication

Not applicable.

Competing interests

No potential conflict of interest was reported by the authors.

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06 Aug, 2023

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Focused Ultrasound versus the Loop Electrosurgical Excision Procedure to Treat Women with Cervical High-grade Squamous Intraepithelial Lesions Under 40: A Retrospective Study

Status:

Journal Publication

Version 1

Abstract

Background

Methods

Results

Conclusion

Figures

Introduction

Methods

Results

Discussion

Conclusions

Abbreviations

Declarations

Acknowledgements

References

Additional Declarations

Status:

Journal Publication

Version 1