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Intravaginal estrogen management in postmenopausal patients with vaginal squamous intraepithelial lesions along with CO2 laser ablation: A retrospective study

  • Shengyao Lei , Congquan Wu , Siyi Zhong , Yanmei Liu , Ke Peng , Xiao Han , Jialing Chen , Chunlan Li EMAIL logo and Shujun Gao EMAIL logo
Published/Copyright: August 8, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

This study aims to investigate the influence of topical estrogen management in postmenopausal patients who had undergone CO2 laser ablation for vaginal squamous intraepithelial lesions (SILs). The clinical data of 211 postmenopausal women with vaginal SILs were reviewed. Patients were divided into two groups by 2-month different management: Group 1 (intervention group): patients were treated with estrogen cream 0.5 g every other day and Group 2 (control group): no topical agent was used for the treatment of patients. In low-grade squamous intraepithelial lesions (LSILs), the response rates for patients in the intervention group and the control group were 49.1% (27/55) and 54.2% (16/48), respectively; human papillomavirus (HPV) status turned negative in 12 (12/38, 31.6%) patients of the intervention group and in 15 (15/35, 42.9%) patients of the control group. In high-grade squamous intraepithelial lesions (HSILs), the response rates for patients in the intervention group and the control group were 72.4% (42/58) and 78.0% (39/50), respectively, nearly 1.5 times higher than those of the LSIL patients; 22 (22/54, 40.7%) patients of the intervention groups and 12 (12/46, 26.1%) patients of the control group cleared the HPV infection. In postmenopausal patients, local use of estrogen cream improves the recognition of lesions and is conducive to precision medicine.

Keywords: vaginal squamous intraepithelial lesion; estrogen; post-menopause

1 Introduction

A vaginal squamous intraepithelial lesion (SIL) is a relatively uncommon disease, with an annual incidence rate of 0.2–2/100,000 [1]. No consensus has been reached on the initial treatment and post-treatment management. CO2 laser ablation has been widely used over the years as a primary treatment due to its safety, minimal invasiveness, repeatability [2], and effectiveness [3,4]. However, studies revealed that vaginal SIL had a high recurrence rate (3.5–13.8%), persistence rate (6.4–13.8%), and malignant progression rate (2–14.3%) in the menopausal period [1,5,6]. Vaginal SIL tends to develop during women’s menopausal period [7,8]. Long-term follow-up results supported that menopausal status was a risk factor for vaginal SIL progression (odds ratio = 10.8; 95% CI = 1.3–87.5) [9]. The evidence above suggests that lower estrogen levels could be a potential risk factor for postmenopausal women affecting CO2 laser ablation efficacy [10,11]. Usually, estrogen supplement is used to alleviate postmenopausal-associated symptoms [12], but as adjuvant therapy for vaginal SIL, its efficacy must be further evaluated. So far, one retrospective study assessed the outcomes of patients treated for only vaginal high-grade squamous intraepithelial lesions (HSILs), with intravaginal estrogen alone and other treatment modalities (including ablation) with estrogen or not. Although their findings suggested that intravaginal estrogen was potential, no detail was provided about the proportion and effect of each modality [13]. Considering the confounding factors in their outcomes, the impact of topical estrogen on vaginal SIL after CO2 laser ablation is still unclear.

Persistent high-risk (H-R) HPV infection plays an important role in precancerous and cancerous lesions of the vagina [14]. Currently, attention has been devoted to addressing that HPV infection and cervical lesions prefer a vaginal dysbiosis characterized by depleted lactobacilli [15]. Estrogen can positively influence the dominance of lactobacilli to help HPV clearance [10]. To date, few studies have taken care of whether vaginal estrogen medication could help the prognosis of vaginal SIL and HPV clearance among postmenopausal women.

To better understand the effect of estrogen administration on HPV clearance and treatment efficacy, we retrospectively analyzed 211 postmenopausal vaginal SIL patients who received CO2 laser surgery (combined with or without estrogen administration).

2 Materials and methods

2.1 Patients

The clinical data of 211 postmenopausal patients were reviewed from May 2020 to August 2020 in the Center of Diagnosis and Treatment of Cervical Disease, Obstetrics and Gynecology Hospital of Fudan University. Inclusion criteria are as follows: (1) postmenopausal women, (2) proven vaginal SIL by histopathology and the highest-grade lesion was recorded as the final pathologic diagnosis when a range of severity on biopsy, (3) received CO2 laser ablation as the initial treatment modality. Exclusion criteria are as follows: (1) more than 70 years old; (2) suspected of invasive vaginal cancer or with vaginal cancer medical history; (3) with or suspected of estrogen-dependent tumors (endometrial cancer, breast cancer, etc.) as well as endometrial dysplasia; (4) with contraindications for intravaginal estrogen or Lactobacillus; (5) with contraindications for CO2 laser ablation; (6) with thrombophlebitis or thromboembolic diseases; and (7) unavailable for surveillance. Finally, 211 participants were eligible for analysis (Figure 1).

Figure 1 Study flow chart. Abbreviation: OGHFU, Obstetrics and Gynecology Hospital of Fudan University; HPV, human papillomavirus; LBC, liquid-based cytology; COVID-19, corona virus disease 2019.
Figure 1

Study flow chart. Abbreviation: OGHFU, Obstetrics and Gynecology Hospital of Fudan University; HPV, human papillomavirus; LBC, liquid-based cytology; COVID-19, corona virus disease 2019.

  1. Informed consent: Informed consent has been obtained from all individuals included in this study.

  2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance with the tenets of the Helsinki Declaration, and has been approved by the Ethics Committee of the Obstetrics and Gynecology Hospital of Fudan University.

2.2 Agent and groups

During the 2-month management since 1 week before the laser operation, some patients used the vaginal estrogen cream, Conjugated Estrogens Cream, Honglilai® (batch number: H20051718), containing 0.625 mg/g estrogen, which has been approved by the China Food and Drug Administration and was widely demonstrated to be safe and effective in helping the vaginal microenvironment in the short term. According to different management strategies, patients were divided into two groups: Group 1 (intervention group): patients were treated with intravaginal estrogen cream 0.5 g every other day; Group 2 (control group): patients were treated by observation only.

2.3 Surveillance

Surveillance, including human papillomavirus (HPV) testing, cytology results, and colposcopy histopathology, was finished 6 months after the CO2 laser ablation operation to assess the efficacy of the topical agent. Generally, surveillance should be done in the same medical center. However, a few patients were followed up nearby due to the COVID-19 pandemic. Their data were collected by telephone interviews.

2.4 Cytology

Liquid-based cytology (LBC) samples collected by experienced gynecologists from the cervical transformation area and the posterior vaginal fornix or vaginal roof were obtained with the SurePath platform (BD Diagnostics) rotating 5–10 turns in the same direction to ensure sufficient number of cells. The sample preparation process in the pathology laboratory was strictly monitored. Cytology results were interpreted and reported by two senior pathologists referring to the 2014 Bethesda System. Slides were reviewed again, and a consensus diagnosis was obtained when differences arose.

2.5 HPV testing

HPV testing in the pathology laboratory was performed using a fluorescence-based multiplex real-time HPV DNA genotyping kit (Bioperfectus, Jiangsu, China), which could detect the 14 high-risk HPV genotypes (HPV-16, -18, -31, -33, -35, -39, -45, -51, -52, -56, -58, 59, -66, and -68) with the same sample cells collection method as cytology.

2.6 Colposcopy and biopsy

Patients received a colposcopy evaluation 6 months after finishing the initial CO2 laser ablation operation. In our research, the Leisegang d-10625 colposcope was used by a specialist to inspect the vulva, vagina, and cervix (if present) according to the manufacturer’s instructions. Tissues showing a white appearance with acetic acid, abnormal blood vessels, non-iodine-staining parts, and suspicious lesions were biopsied and then sent for histopathological examination in the pathology laboratory. Two senior gynecologic pathologists made the diagnosis according to the fourth edition of the World Health Organization (WHO) Classification of Female Genital Tumors.

2.7 Observation of clinical therapeutic effects

By comprehensively measuring the laboratory results and biopsy diagnoses before and after treatment, we developed a form of vaginal SIL outcome. Four types of classifications were used: cure, remission, persistence/recurrence, and progression. Among them, the former two were considered effective outcomes, and the remaining were ineffective; more details are provided in Table 1. The primary outcome was to evaluate the rate of effectiveness. The secondary outcome measured the HPV clearance rate.

Table 1

Vaginal SIL outcome evaluation form

Pathology of colposcopy biopsy Cytology HPV infection Cervix excision Outcome
Lesion positive Downgrade* / / / Remission
Same-grade* Downgrade* / / Persistence/recurrence
Same-grade* Upgrade* / / Progression
Upgrade* / / / Progression
Lesion negative ≤ASCUS N / Cure
≤ASCUS Y / Cure (persistent HPV infection)
>ASCUS / N Cure (abnormal cells from cervix)
Same-grade* / Y Persistence/recurrence
Upgrade* / Y Progression

Y: yes. N: no. /: not be considered. *: compared with the results before CO2 laser ablation. ASCUS: atypical squamous cell of undetermined significance.

2.8 Statistical analysis

Statistical analysis was performed using SPSS (version 26.0; SPSS, Inc., Chicago, USA), indicated as mean (SD) or number (%) of cases, if necessary. Pearson’s chi-square test and Fisher’s exact test were adopted to compare the rates among the groups when suitable. Kendall’s tau method was used to reveal the relationship between lesion severity and efficacy. All tests used were two-tailed. Statistical significance was set at P < 0.05.

3 Results

Medical records were evaluated for demographic and histopathological characteristics of patients, as presented in Table 2. A total of 211 postmenopausal patients were included in the analysis, 103 vaginal LSIL patients (55 in Group 1, 48 in Group 2), and 108 HSIL patients (58 in Group 1, 50 in Group 2). Four of the HSIL patients (two in Group 1, two in Group 2) developed invasive vaginal cancer; the malignancy rate was 1.9% (4/211). The age range of the study population was 48–69 years, with the median age of diagnosis of 58 years (58 ± 5.4). No difference was found in the following aspects: age at the first sexual intercourse, number of sexual partners, the mode of delivery, and smoking. In our study, patients with cervical lesion history were more likely to suffer from vaginal HSIL. Compared with LSIL patients, the number of patients with cervical HSIL history in vaginal HSIL was more than twice (P = 0.001), and the number of patients with cervical cancer history was nearly ten times (P < 0.001). Previous studies [16,17] indicated the association between cervical lesions and vaginal intraepithelial neoplasia. Furthermore, we found that cervical HSIL and cervical cancer could increase the severity of vaginal SIL, with correlation coefficient (CC) values of 0.21 (P = 0.01) and 0.224 (P < 0.001), respectively. In addition, H-R HPV-positive patients accounted for nearly 90% in the HSIL group while accounting for slightly more than 70% (P < 0.001). The multiple infection rates in different pathological groups were not significantly different.

Table 2

Clinical characteristics of the postmenopausal patients with vaginal SIL

Clinical characteristics LSIL (103) HSIL (108) P-Value
Age (mean + SD, years) 58.3 ± 5.4 53.9 ± 9.5 <0.001
Age of first sexual intercourse (mean + SD, years) 23 ± 2.5 23 ± 2.5 0.548
Amount of sexual partners (mean + SD) 1.4 ± 0.6 1.5 ± 0.7 0.793
Smoking (n, %) 0.648
Yes 1 (0.01%) 3 (2.8%)
No 102 (99.9%) 105 (97.2%)
History of delivery (n, %) 0.433
Natural delivery 90 (87.4%) 98 (90.7%)
Cesarean delivery 13 (12.6%) 10 (9.3%)
History of hysterectomy (n, %) 0.002
Positive 32 (31.1%) 56 (51.9%)
Negative 71 (68.9%) 52 (48.1%)
History cervical HSIL (n, %) 0.001
Positive 15 (14.6%) 35 (32.4%)
Negative 88 (85.4%) 73 (67.6%)
History cervical cancer (n, %) <0.001
Positive 2 (1.9%) 19 (17.6%)
Negative 101 (98.1%) 89 (82.4%)
H-R HPV (n, %) <0.001
Positive 73 (70.9%) 100 (92.6%)
Negative 30 (29.1%) 8 (7.4%)
H-R HPV positive (n, %) 0.135
Single infection 40 (54.8%) 66 (66.3%)
Multiple infection 33 (45.2%) 34 (33.7%)

H-R: high risk. LSIL: low-grade squamous intraepithelial lesion. HSIL: high-grade squamous intraepithelial lesion.

Table 3 shows the efficacy evaluation of the two adjuvant treatments after laser ablation. Overall, cure was the primary outcome in different pathological groups regardless of intravaginal medication, which fluctuated from 45% to 55%. Among LSIL patients, the effective rate was 49.1% in the intervention group and 54.2% in the control group (P = 0.607); among HSIL patients, the effective rate was 72.4% in the intervention group and 78.0% in the control group (P = 0.504). The aforementioned results might suggest that: in different pathological subgroups, estrogen cream could not improve the curative effect. Among patients who received vaginal medication, the response rate was 72.4% (42/58) for HSIL patients and 49.1% (27/55) for LSIL patients (P = 0.011); in patients treated by observation, the response rate was 78.0% (39/50) for HSIL patients and 54.2% (26/48) for LSIL patients (P = 0.013). The evidence above might further indicate that the response rate for HSIL patients would always be better than that of LSIL patients, which is about 1.5 times that of LSIL patients.

Table 3

Outcomes of patients with different vaginal SIL after postoperative management

Groups (n) Treatment outcomes (n, %) Effect (n, %)
Cure Regression Persistence* Progression Effectivea Ineffectiveb
LSIL
Group 1 (55) 27 (49.1) 0 (0.0) 16 (29.1) 12 (21.8) 27 (49.1) 28 (50.9)
Group 2 (48) 26 (54.2) 0 (0.0) 17 (35.4) 5 (10.4) 26 (54.2) 22 (45.8)
Total (103) 53 (51.0) 0 (0.0) 33 (33.0) 17 (16.0) 53 (51.0) 50 (49.0)
HSIL
Group 1 (58) 29 (50.0) 13 (22.4) 12 (20.7) 4 (6.9) 42 (72.4) 16 (27.6)
Group 2 (50) 22 (44.0) 17 (34.0) 7 (14.0) 4 (8.0) 39 (78.0) 11 (22.0)
Total (108) 51 (47.2) 30 (27.6) 19 (17.6) 8 (7.6) 81 (74.8) 27 (25.2)

Group 1: intravaginal estrogen cream 0.5 g every other day; Group 2: no topical agent.

Persistence*: including persistence and recurrence; effectivea: including cure and regression.

Ineffectiveb: including persistence, recurrence and progression.

p effect = 0.986 when “Group 1 of LSIL” versus “Group 2 of LSIL.”

p effect = 0.504 when “Group 1 of HSIL” versus “Group 2 of HSIL.”

p effect = 0.030 when “Group 1 of LSIL” versus “Group 1 of HSIL.”

p effect = 0.013 when “Group 2 of LSIL” versus “Group 2 of HSIL.”

HPV clearance outcomes of the two groups are given in Table 4. Among all patients included in the analysis, the HPV clearance rate of the estrogen cream users was slightly higher (37.0%, 34/92) than that of the observation group ones (33.3%, 27/81). However, the difference was not statistically significant (P = 0.619). By ranking the HPV clearance rate, we found that the order of HPV clearance ability from high to low was Group 2 of LSIL (42.9%, 15/35), Group 1 of HSIL (40.7%, 22/54), Group 1 of LSIL (31.6%, 12/38), and Group 2 of HSIL (21.6%, 12/46). We also stratified analysis of the HPV clearance ability in the four subgroups, but all comparisons did not reveal statistical differences in disease severity and medication.

Table 4

HPV status of patients with different vaginal SIL after postoperative management

Group (n) Turned negative (n, %) Persistently positive (n, %) Turn negative rate
Single Multiple Single Multiple
LSIL
Group 1 (38) 9 (75.0) 3 (25.0) 11 (42.3) 15 (57.7） 31.2% (12/38)
Group 2 (35) 10 (66.7) 5 (23.3) 10 (50.0) 10 (50.0) 42.9% (15/35)
Total (73) 19 (70.3) 8 (29.7) 21 (45.6) 25 (54.4) 36.99% (27/73)
HSIL
Group 1 (54) 15 (68.2) 7 (31.8) 24 (75.0) 8 (25.0) 40.7% (22/54)
Group 2 (46) 11 (91.7) 1 (8.3) 17 (50.0) 17 (50.0) 26.1% (12/46)
Total (100) 26 (76.5) 8 (23.5) 41 (62.1) 25 (37.9) 34% (34/100)

Group 1: intravaginal estrogen cream 0.5 g every other day; Group 2: no topical agent.

P turn nagative rate = 0.178 when “Group 1 of LSIL” versus “Group 2 of LSIL.”

P turn nagative rate = 0.123 when “Group 1 of HSIL” versus “Group 2 of HSIL.”

P turn nagative rate = 0.199 when “Group 1 of LSIL” versus “Group 1 of HSIL.”

P turn nagative rate = 0.113 when “Group 2 of LSIL” versus “Group 2 of HSIL.”

4 Discussion

The clinical characteristics of vaginal HSIL make it easier to be identified [18], which may lead to a better therapeutic effect. High-grade lesions show dense acetowhite epithelium, coarse mosaic, coarse punctation, sharp borders, inner border signs, and ridge signs [19]. All of these features help pinpoint the surgical site and enhance laser efficacy. Consistent with that, the effective rate of HSIL patients was about 1.5 times that of LSIL patients in our study. Since the severity of vaginal lesions was the only significant independent factor of persistence/recurrence after one episode of laser [20], we found a phenomenon that the operators are more inclined to enlarge the ablation extent and depth for patients with vaginal HSIL. According to the above, the importance to a CO2 laser ablation provider’s ability to evaluate the entire vagina of women with vaginal lesions should be attached.

The decision of CO2 laser ablation treatment for vaginal LSIL should be considered. Mengyin Ao et al. [6] retrospectively assessed the largest sample size investigation containing 646 vaginal LSILs with a median follow-up of 14 months (6–60 months). Among the vaginal LSIL patients, none developed invasive vaginal cancer, and the progression rate to vaginal HSIL was 18 (2.8%). Of the 201 LSIL patients treated only by observation, 178 (88.6%) turned to normalization. Since vaginal LSIL generally has a good prognosis [21], it has been suggested that LSIL should be managed conservatively [6,22]. However, in our study population, LSIL patients still had a high progression rate of 49% (50/103). Previous studies have suggested that postmenopausal status, H-R HPV infection, and cervical lesions/cancer history are risk factors for progression [6,9,14,23]. Thus, we recommend active treatments for LSIL women with high risk factors, and more emphasis should be paid to surveillance.

H-R HPV infection is closely associated with high-grade vaginal lesions. H-R HPV was identified in a large proportion of invasive vaginal cancers (70–78%) and almost all vaginal HSILs (92–98%) [14]. In the vaginal HSIL women we reported, the H-R HPV infection rate was as high as 92.6% (100/108). It is well known that postmenopausal women feature estrogen deprivation and Lactobacillus absence in the vaginal ecosystem. Estrogen can help vaginal epithelium proliferation and intracellular glycogen production, increasing Lactobacillus population [24,25]. With the increase in the Lactobacillus population, HPV clearance rate can be significantly improved [26]. We believe that satisfactory management should focus on two aspects: lesion tissue ablation and HPV infection clearance. The latter may be reached through additional supplementation of vaginal probiotics.

In postmenopausal patients, although short-term use of intravaginal estrogen cream does not improve the efficacy of the laser, it can increase satisfaction with lesion identification and accelerate the healing after ablation. The lack of estrogen during menopause may negatively impact the vaginal mucosa, resulting in the reduction of elastin and collagen in vaginal tissue, thinning of the vaginal epithelium, and decrease of glycogen in the epithelium [10,27]. All of those changes negatively affect acetowhite epithelium recognition and degree of staining with iodine, especially in vaginal LSIL patients complicated with atrophic vaginitis (Figure 2). In addition, the ablation site often takes longer to heal. During the healing period, some patients may have local adhesion and stenosis, which may bring difficulties in satisfying exposure of the vagina during follow-up examinations. Yet, as shown in Figure 3, we discovered that topical estrogen cream considerably improves such circumstances. In fact, intravaginal estrogen given before colposcopy can improve the elasticity of mucosal folds [13] and present with more reliable colposcopy results [28]. Additionally, postoperative local estrogen management (which began on the day of operation) also resulted in a marked proliferation of the vaginal epithelial layer and active epithelial barrier function [29]. Until now, available evidence presents a complex relationship between estrogen and HPV, with both carcinogenic and anticancer effects on tumor development [30,31,32], while neutral results are presented for estrogen effects in our study. Given the above advantages, we recommend short-term topical estrogen management as a pre-colposcopy preparation and a restorative medication along with CO2 laser ablation.

Figure 2 The colposcopy images of a 62-year-old patient who was biopsy proved vaginal LSIL and did not use intravaginal estrogen cream. (a) Vagina without the use of estrogen; (b) acetic acid stained (middle and lower region of the right wall); and (c) iodine-stained.
Figure 2

The colposcopy images of a 62-year-old patient who was biopsy proved vaginal LSIL and did not use intravaginal estrogen cream. (a) Vagina without the use of estrogen; (b) acetic acid stained (middle and lower region of the right wall); and (c) iodine-stained.

Figure 3 The colposcopy images of a 67-year-old patient after hysterectomy who was biopsy proved vaginal LSIL after two-weeks intravaginal estrogen cream. (a) Vagina after estrogen used; (b) acetic acid stained (upper region of the left wall); (c) enlarged; and (d) iodine-stained.
Figure 3

The colposcopy images of a 67-year-old patient after hysterectomy who was biopsy proved vaginal LSIL after two-weeks intravaginal estrogen cream. (a) Vagina after estrogen used; (b) acetic acid stained (upper region of the left wall); (c) enlarged; and (d) iodine-stained.

To our best knowledge, this is the largest retrospective study focusing on the potential benefits of using topical estrogen agents along with CO2 laser ablation among postmenopausal vaginal SIL patients. Our study is limited. Our sample size is not large enough; further sample collections and elongated follow-up periods may be essential for more accurate analysis. Nevertheless, our study provided a comprehensive analysis, which could add a meaningful insight into vaginal SIL management.

5 Conclusions

The treatment of vaginal HSIL in postmenopausal patients with CO2 ablation is effective. Short-term intravaginal estrogen combined with CO2 laser ablation does not significantly improve the treatment efficacy. Applying estrogen cream locally helps lesion identification under colposcopy and promotes precise treatment.

# Co-first authors, contributed equally to this work.

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  1. Funding information: This work was supported by the Natural Science Fund of Shanghai Science and Technology Committee (17ZR1403400) to S.G.

  2. Author contributions: Shengyao Lei was responsible for drafting the manuscript. Shengyao Lei and Congquan Wu contributed to the analysis and interpretation of data. Siyi Zhong, Yanmei Liu, Ke Peng, Xiao Han and Jialing Chen contributed to the data collection. All authors read and approved the final manuscript.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2023-02-17
Revised: 2023-04-08
Accepted: 2023-04-27
Published Online: 2023-08-08

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0621
Keywords for this article
vaginal squamous intraepithelial lesion; estrogen; post-menopause
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Systemic investigation of inetetamab in combination with small molecules to treat HER2-overexpressing breast and gastric cancers
  3. Immunosuppressive treatment for idiopathic membranous nephropathy: An updated network meta-analysis
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  23. Refractory hypokalemia with sexual dysplasia and infertility caused by 17α-hydroxylase deficiency and triple X syndrome: A case report
  24. Meta-analysis of cancer risk among end stage renal disease undergoing maintenance dialysis
  25. 6-Phosphogluconate dehydrogenase inhibition arrests growth and induces apoptosis in gastric cancer via AMPK activation and oxidative stress
  26. Experimental study on the optimization of ANM33 release in foam cells
  27. Primary retroperitoneal angiosarcoma: A case report
  28. Metabolomic analysis-identified 2-hydroxybutyric acid might be a key metabolite of severe preeclampsia
  29. Malignant pleural effusion diagnosis and therapy
  30. Effect of spaceflight on the phenotype and proteome of Escherichia coli
  31. Comparison of immunotherapy combined with stereotactic radiotherapy and targeted therapy for patients with brain metastases: A systemic review and meta-analysis
  32. Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation
  33. Association between the VEGFR-2 -604T/C polymorphism (rs2071559) and type 2 diabetic retinopathy
  34. The role of IL-31 and IL-34 in the diagnosis and treatment of chronic periodontitis
  35. Triple-negative mouse breast cancer initiating cells show high expression of beta1 integrin and increased malignant features
  36. mNGS facilitates the accurate diagnosis and antibiotic treatment of suspicious critical CNS infection in real practice: A retrospective study
  37. The apatinib and pemetrexed combination has antitumor and antiangiogenic effects against NSCLC
  38. Radiotherapy for primary thyroid adenoid cystic carcinoma
  39. Design and functional preliminary investigation of recombinant antigen EgG1Y162–EgG1Y162 against Echinococcus granulosus
  40. Effects of losartan in patients with NAFLD: A meta-analysis of randomized controlled trial
  41. Bibliometric analysis of METTL3: Current perspectives, highlights, and trending topics
  42. Performance comparison of three scaling algorithms in NMR-based metabolomics analysis
  43. PI3K/AKT/mTOR pathway and its related molecules participate in PROK1 silence-induced anti-tumor effects on pancreatic cancer
  44. The altered expression of cytoskeletal and synaptic remodeling proteins during epilepsy
  45. Effects of pegylated recombinant human granulocyte colony-stimulating factor on lymphocytes and white blood cells of patients with malignant tumor
  46. Prostatitis as initial manifestation of Chlamydia psittaci pneumonia diagnosed by metagenome next-generation sequencing: A case report
  47. NUDT21 relieves sevoflurane-induced neurological damage in rats by down-regulating LIMK2
  48. Association of interleukin-10 rs1800896, rs1800872, and interleukin-6 rs1800795 polymorphisms with squamous cell carcinoma risk: A meta-analysis
  49. Exosomal HBV-DNA for diagnosis and treatment monitoring of chronic hepatitis B
  50. Shear stress leads to the dysfunction of endothelial cells through the Cav-1-mediated KLF2/eNOS/ERK signaling pathway under physiological conditions
  51. Interaction between the PI3K/AKT pathway and mitochondrial autophagy in macrophages and the leukocyte count in rats with LPS-induced pulmonary infection
  52. Meta-analysis of the rs231775 locus polymorphism in the CTLA-4 gene and the susceptibility to Graves’ disease in children
  53. Cloning, subcellular localization and expression of phosphate transporter gene HvPT6 of hulless barley
  54. Coptisine mitigates diabetic nephropathy via repressing the NRLP3 inflammasome
  55. Significant elevated CXCL14 and decreased IL-39 levels in patients with tuberculosis
  56. Whole-exome sequencing applications in prenatal diagnosis of fetal bowel dilatation
  57. Gemella morbillorum infective endocarditis: A case report and literature review
  58. An unusual ectopic thymoma clonal evolution analysis: A case report
  59. Severe cumulative skin toxicity during toripalimab combined with vemurafenib following toripalimab alone
  60. Detection of V. vulnificus septic shock with ARDS using mNGS
  61. Novel rare genetic variants of familial and sporadic pulmonary atresia identified by whole-exome sequencing
  62. The influence and mechanistic action of sperm DNA fragmentation index on the outcomes of assisted reproduction technology
  63. Novel compound heterozygous mutations in TELO2 in an infant with You-Hoover-Fong syndrome: A case report and literature review
  64. ctDNA as a prognostic biomarker in resectable CLM: Systematic review and meta-analysis
  65. Diagnosis of primary amoebic meningoencephalitis by metagenomic next-generation sequencing: A case report
  66. Phylogenetic analysis of promoter regions of human Dolichol kinase (DOLK) and orthologous genes using bioinformatics tools
  67. Collagen changes in rabbit conjunctiva after conjunctival crosslinking
  68. Effects of NM23 transfection of human gastric carcinoma cells in mice
  69. Oral nifedipine and phytosterol, intravenous nicardipine, and oral nifedipine only: Three-arm, retrospective, cohort study for management of severe preeclampsia
  70. Case report of hepatic retiform hemangioendothelioma: A rare tumor treated with ultrasound-guided microwave ablation
  71. Curcumin induces apoptosis in human hepatocellular carcinoma cells by decreasing the expression of STAT3/VEGF/HIF-1α signaling
  72. Rare presentation of double-clonal Waldenström macroglobulinemia with pulmonary embolism: A case report
  73. Giant duplication of the transverse colon in an adult: A case report and literature review
  74. Ectopic thyroid tissue in the breast: A case report
  75. SDR16C5 promotes proliferation and migration and inhibits apoptosis in pancreatic cancer
  76. Vaginal metastasis from breast cancer: A case report
  77. Screening of the best time window for MSC transplantation to treat acute myocardial infarction with SDF-1α antibody-loaded targeted ultrasonic microbubbles: An in vivo study in miniswine
  78. Inhibition of TAZ impairs the migration ability of melanoma cells
  79. Molecular complexity analysis of the diagnosis of Gitelman syndrome in China
  80. Effects of maternal calcium and protein intake on the development and bone metabolism of offspring mice
  81. Identification of winter wheat pests and diseases based on improved convolutional neural network
  82. Ultra-multiplex PCR technique to guide treatment of Aspergillus-infected aortic valve prostheses
  83. Virtual high-throughput screening: Potential inhibitors targeting aminopeptidase N (CD13) and PIKfyve for SARS-CoV-2
  84. Immune checkpoint inhibitors in cancer patients with COVID-19
  85. Utility of methylene blue mixed with autologous blood in preoperative localization of pulmonary nodules and masses
  86. Integrated analysis of the microbiome and transcriptome in stomach adenocarcinoma
  87. Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy
  88. DUSP2 inhibits the progression of lupus nephritis in mice by regulating the STAT3 pathway
  89. Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series
  90. Genetic alterations of KRAS and TP53 in intrahepatic cholangiocarcinoma associated with poor prognosis
  91. Granulomatous polyangiitis involving the fourth ventricle: Report of a rare case and a literature review
  92. Studying infant mortality: A demographic analysis based on data mining models
  93. Metaplastic breast carcinoma with osseous differentiation: A report of a rare case and literature review
  94. Protein Z modulates the metastasis of lung adenocarcinoma cells
  95. Inhibition of pyroptosis and apoptosis by capsaicin protects against LPS-induced acute kidney injury through TRPV1/UCP2 axis in vitro
  96. TAK-242, a toll-like receptor 4 antagonist, against brain injury by alleviates autophagy and inflammation in rats
  97. Primary mediastinum Ewing’s sarcoma with pleural effusion: A case report and literature review
  98. Association of ADRB2 gene polymorphisms and intestinal microbiota in Chinese Han adolescents
  99. Tanshinone IIA alleviates chondrocyte apoptosis and extracellular matrix degeneration by inhibiting ferroptosis
  100. Study on the cytokines related to SARS-Cov-2 in testicular cells and the interaction network between cells based on scRNA-seq data
  101. Effect of periostin on bone metabolic and autophagy factors during tooth eruption in mice
  102. HP1 induces ferroptosis of renal tubular epithelial cells through NRF2 pathway in diabetic nephropathy
  103. Intravaginal estrogen management in postmenopausal patients with vaginal squamous intraepithelial lesions along with CO2 laser ablation: A retrospective study
  104. Hepatocellular carcinoma cell differentiation trajectory predicts immunotherapy, potential therapeutic drugs, and prognosis of patients
  105. Effects of physical exercise on biomarkers of oxidative stress in healthy subjects: A meta-analysis of randomized controlled trials
  106. Identification of lysosome-related genes in connection with prognosis and immune cell infiltration for drug candidates in head and neck cancer
  107. Development of an instrument-free and low-cost ELISA dot-blot test to detect antibodies against SARS-CoV-2
  108. Research progress on gas signal molecular therapy for Parkinson’s disease
  109. Adiponectin inhibits TGF-β1-induced skin fibroblast proliferation and phenotype transformation via the p38 MAPK signaling pathway
  110. The G protein-coupled receptor-related gene signatures for predicting prognosis and immunotherapy response in bladder urothelial carcinoma
  111. α-Fetoprotein contributes to the malignant biological properties of AFP-producing gastric cancer
  112. CXCL12/CXCR4/CXCR7 axis in placenta tissues of patients with placenta previa
  113. Association between thyroid stimulating hormone levels and papillary thyroid cancer risk: A meta-analysis
  114. Significance of sTREM-1 and sST2 combined diagnosis for sepsis detection and prognosis prediction
  115. Diagnostic value of serum neuroactive substances in the acute exacerbation of chronic obstructive pulmonary disease complicated with depression
  116. Research progress of AMP-activated protein kinase and cardiac aging
  117. TRIM29 knockdown prevented the colon cancer progression through decreasing the ubiquitination levels of KRT5
  118. Cross-talk between gut microbiota and liver steatosis: Complications and therapeutic target
  119. Metastasis from small cell lung cancer to ovary: A case report
  120. The early diagnosis and pathogenic mechanisms of sepsis-related acute kidney injury
  121. The effect of NK cell therapy on sepsis secondary to lung cancer: A case report
  122. Erianin alleviates collagen-induced arthritis in mice by inhibiting Th17 cell differentiation
  123. Loss of ACOX1 in clear cell renal cell carcinoma and its correlation with clinical features
  124. Signalling pathways in the osteogenic differentiation of periodontal ligament stem cells
  125. Crosstalk between lactic acid and immune regulation and its value in the diagnosis and treatment of liver failure
  126. Clinicopathological features and differential diagnosis of gastric pleomorphic giant cell carcinoma
  127. Traumatic brain injury and rTMS-ERPs: Case report and literature review
  128. Extracellular fibrin promotes non-small cell lung cancer progression through integrin β1/PTEN/AKT signaling
  129. Knockdown of DLK4 inhibits non-small cell lung cancer tumor growth by downregulating CKS2
  130. The co-expression pattern of VEGFR-2 with indicators related to proliferation, apoptosis, and differentiation of anagen hair follicles
  131. Inflammation-related signaling pathways in tendinopathy
  132. CD4+ T cell count in HIV/TB co-infection and co-occurrence with HL: Case report and literature review
  133. Clinical analysis of severe Chlamydia psittaci pneumonia: Case series study
  134. Bioinformatics analysis to identify potential biomarkers for the pulmonary artery hypertension associated with the basement membrane
  135. Influence of MTHFR polymorphism, alone or in combination with smoking and alcohol consumption, on cancer susceptibility
  136. Catharanthus roseus (L.) G. Don counteracts the ampicillin resistance in multiple antibiotic-resistant Staphylococcus aureus by downregulation of PBP2a synthesis
  137. Combination of a bronchogenic cyst in the thoracic spinal canal with chronic myelocytic leukemia
  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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