Lu JJ, Yan S, Chen L, Ju LL, Cai WH, Wu JZ. Retrospective analysis of patients with hepatocellular carcinoma complicated with human immunodeficiency virus infection after hepatectomy. World J Gastrointest Oncol 2024; 16(9): 3851-3864 [DOI: 10.4251/wjgo.v16.i9.3851]
Corresponding Author of This Article
Jin-Zhu Wu, MD, Chief, Chief Doctor, Professor, Department of Hepatobiliary Surgery, Affiliated Nantong Hospital 3 of Nantong University, No. 19 Qixiu Road, Chongchuan District, Nantong 226006, Jiangsu Province, China. wjz1258@163.com
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Retrospective Cohort Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Jia-Jie Lu, Department of Hepatobiliary Surgery, Nantong Third People's Hospital, Medical School of Nantong University, Nantong 226000, Jiangsu Province, China
Shuai Yan, Department of Medical School, Nantong University, Nantong 226300, Jiangsu Province, China
Lin Chen, Lin-Ling Ju, Institute of Liver Disease, Nantong Third People’s Hospital, Affiliated Nantong Hospital 3 of Nantong University, Nantong 226000, Jiangsu Province, China
Wei-Hua Cai, Jin-Zhu Wu, Department of Hepatobiliary Surgery, Affiliated Nantong Hospital 3 of Nantong University, Nantong 226006, Jiangsu Province, China
Author contributions: Lu JJ wrote the paper; Yan S analyzed the data and outcomes; Chen L contributed analytic tools; Ju LL collected the data; Cai WH contributed new reagents; Wu JZ designed the research; all authors have read and approved the final version. Lu JJ and Yan S contributed equally to this work as co-first authors. There are three reasons for appointing Lu JJ and Yan S as co-first authors. First, the study was conducted as a collaborative effort, and the designation of co-first author accurately reflects the allocation of responsibilities and burdens associated with the time and effort required to complete the research and final paper. This also ensures effective communication and management of post-submission transactions, ultimately improving the quality and reliability of the paper. Second, the entire research team includes authors with a wide range of expertise and skills from different fields, and the designation of co-first author best reflects this diversity. This also promotes the most comprehensive and in-depth examination of the research topic, ultimately enriching the reader's understanding by providing a variety of expert perspectives. Third, Lu JJ and Yan S made equally important contributions in the whole research process. The selection of these researchers as co-first authors is a recognition and respect for their equal contribution, as well as a recognition of the teamwork spirit of this research. To sum up, we feel that the designation of Lu JJ and Yan S as co-first authors is appropriate for our manuscript, as it accurately reflects our team's spirit of cooperation, equal contribution and diversity.
Supported byNantong Municipal Health Commission, No. MSZ2022036.
Institutional review board statement: The study was reviewed and approved by the Institutional Review Board.
Informed consent statement: All study participants or their legal guardian provided informed written consent about personal and medical data collection prior to study enrolment.
Conflict-of-interest statement: The authors declare no competing interests. All authors issued final approval for the version to be submitted for publication.
Data sharing statement: Enquiries about data access should be made to the corresponding author.
STROBE statement: The authors have read the STROBE Statement—checklist of items, and the manuscript was prepared and revised according to the STROBE Statement—checklist of items.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Jin-Zhu Wu, MD, Chief, Chief Doctor, Professor, Department of Hepatobiliary Surgery, Affiliated Nantong Hospital 3 of Nantong University, No. 19 Qixiu Road, Chongchuan District, Nantong 226006, Jiangsu Province, China. wjz1258@163.com
Received: May 12, 2024 Revised: July 30, 2024 Accepted: August 15, 2024 Published online: September 15, 2024 Processing time: 119 Days and 16.7 Hours
Abstract
BACKGROUND
Hepatocellular carcinoma (HCC) is the third leading cause of cancer death worldwide, with a 5-year relative survival rate of approximately 18%. The similarity between incidence and mortality (830000 deaths per year) underscores the bleak prognosis associated with the disease. HCC is the fourth most common malignancy and the second leading cause of cancer death in China. Most patients with HCC have a history of chronic liver disease such as chronic hepatitis B virus (HBV) or hepatitis C virus (HCV) infection, alcoholism or alcoholic steatohepatitis, nonalcoholic fatty liver disease, or nonalcoholic steatohepatitis. Early diagnosis and effective treatment are the keys to improving the prognosis of patients with HCC. Although the total number of human immunodeficiency virus (HIV)-infected patients is declining globally the incidence of HCC is increasing in HIV-infected patients, especially those who are coinfected with HBV or HCV. As a result, people infected with HIV still face unique challenges in terms of their risk of developing HCC.
AIM
To investigate the survival prognosis and clinical efficacy of surgical resection in patients with HCC complicated with HIV infection.
METHODS
The clinical data of 56 patients with HCC complicated with HIV admitted to the Third Affiliated Hospital of Nantong University from January 2013 to December 2023 were retrospectively analyzed. Among these, 27 patients underwent hepatectomy (operation group) and 29 patients received conservative treatment (nonoperation group). All patients signed informed consents in line with the provisions of medical ethics. The general data, clinicopathological features and prognoses for the patients in the two groups were analyzed and the risk factors related to the prognoses of the patients in the operation group were identified.
RESULTS
The median disease-free survival (DFS) and overall survival (OS) of HIV-HCC patients in the surgical group were 13 months and 17 months, respectively, and the median OS of patients in the nonsurgical group was 12 months. The OS of the surgical group was significantly longer than that of the control group (17 months vs 12 months, respectively; P < 0.05). The risk factors associated with DFS and OS in the surgical group were initial HIV diagnosis, postoperative microvascular invasion (MVI), a CD4+ T-cell count < 200/μL, Barcelona stage C-D, and men who have sex with men (MSM; P < 0.05).
CONCLUSION
Hepatectomy can effectively prolong the survival of patients with HIV-HCC but MVI identified during postoperative pathological examination, late tumor detection, late BCLC stage, CD4+ T < 200/μL and MSM are risk factors affecting the survival and prognosis of patients undergoing hepatectomy. In addition, there were significant differences between the surgical group and the nonsurgical group in terms of the initial diagnosis of HIV, Child-Pugh score, alpha-fetoprotein measurement value, and HART-efficient antiretroviral therapy after the diagnosis of HIV (P < 0.05). Therefore, these factors may also affect the survival and prognosis of patients.
Core Tip: Human immunodeficiency virus (HIV) infection significantly influences treatment strategies for hepatocellular carcinoma (HCC). When developing treatment plans, health care workers must consider the complexity of the immune status of HIV-infected patients and the potential drug interactions resulting from antiretroviral therapy. For HIV-positive HCC patients, HIV infection itself may influence tumor biology and patient response to treatment, thus affecting the cure, recurrence, and long-term survival rates of the disease. Therefore, health care professionals treating HIV-HCC patients must collaborate across disciplines to thoroughly understand the patient's overall condition and develop a comprehensive, personalized treatment plan. To effectively control HIV infection, HCC should be treated and the quality of life of patients should be optimized.
Citation: Lu JJ, Yan S, Chen L, Ju LL, Cai WH, Wu JZ. Retrospective analysis of patients with hepatocellular carcinoma complicated with human immunodeficiency virus infection after hepatectomy. World J Gastrointest Oncol 2024; 16(9): 3851-3864
Hepatocellular carcinoma (HCC) is the third leading cause of cancer death worldwide with a 5-year relative survival rate of approximately 18%. The similarity between morbidity and mortality (830000 deaths per year) underscores the bleak prognosis associated with the disease[1]. HCC is the fourth most common malignant tumor and the second leading cause of cancer death in China[2]. Most patients with HCC have a history of chronic liver disease such as chronic infection with hepatitis B virus (HBV) or hepatitis C virus (HCV), alcoholism or alcoholic steatohepatitis, nonalcoholic fatty liver disease or nonalcoholic steatohepatitis. Early diagnosis and effective treatment are essential for improving the prognosis of patients with HCC[3,4]. Although the total number of HIV-infected patients is declining globally the incidence of HCC in HIV-infected patients has increased, especially for those who are simultaneously infected with HBV or HCV[1]. Therefore, people infected with human immunodeficiency virus (HIV) still face unique challenges in terms of the risk of developing HCC. Although it is still uncertain whether HIV infection directly leads to the occurrence of HCC it may indirectly increase the risk of HCC by affecting the function of the immune system and reducing the immune surveillance of tumor cells[5]. Therefore, active antiretroviral therapy (ART) for HIV-infected patients and regular screening of hepatitis and tumor markers are essential for the prevention of HCC. With improvements in the effectiveness of highly active ART (HAART), HIV can be effectively controlled but the prevalence of HCC has not decreased significantly[6-8]. One of the main reasons is that with the effective control of HIV the probability of death of such patients due to related complications is gradually reduced and their lifespan is prolonged. In turn, inflammation and immune damage prolong the stimulation time for liver tissue in such patients and the probability of carcinogenesis increases[9]. At present, we only have case reports and regional small sample sizes to provide a reference for such patients and most of the data are from Western HCC patients with HCV infection. This type of hepatitis background is very different from the background of HBV infection in the vast majority of HCC patients in China[4,10]. There are no corresponding data supporting whether such patients have similarities and differences with HIV-negative patients or Western patients in terms of screening, diagnosis and treatment programs, and prognosis. There is a serious lack of diagnostic and treatment norms or guidelines for such patients to guide their diagnosis and treatment process. Therefore, this study summarizes and analyzes the clinical data of liver cancer patients with HIV infection at Nantong Third Hospital Affiliated with Nantong University over the past 10 years and compares them with relevant literature at home and abroad to explore preliminarily the clinical characteristics and prognostic factors of such patients.
MATERIALS AND METHODS
The clinical data for 56 patients with HCC complicated with HIV and admitted to the Third Affiliated Hospital of Nantong University from January 2013 to December 2023 were retrospectively analyzed. Among these, 27 patients underwent hepatectomy (operation group) and 29 patients received conservative treatment (nonoperation group). All patients signed informed consents in line with the provisions of medical ethics. The general data, clinicopathological features and prognoses of the patients in the two groups were analyzed, and risk factors related to the prognosis of the patients in the operation group were identified (Figure 1). The detailed clinical and tumor characteristics for the patients, as well as information regarding surgery and prognosis were also considered (Table 1 and Table 2).
Figure 1 Retrospective analysis flowchart for hepatocellular carcinoma patients with human immunodeficiency virus infection after hepatectomy.
HCC: Hepatocellular carcinoma; HIV: Human immunodeficiency virus; OS: Overall survival; DFS: Disease-free survival.
Table 1 Clinical data for patients in the surgery group.
Indicator
n = 27
Age (years)
60.15 ± 5.90
Gender (Male:female)
24:3
HIV initial diagnosis, n (%)
20 (74.1)
HIV-RNA positive, n (%)
13 (48.1)
MSM, n (%)
18 (66.7)
Received HART after HIV diagnosis
21 (77.8)
HBV, n (%)
21 (77.8)
HCV, n (%)
2 (7.4)
Chronic alcohol consumption, n (%)
11 (40.7)
PS score (0-1:2-3)
16:11
CD4+ cell count < 200 (cell/μL)
15 (55.6)
Child-Pugh score (A:B)
21:6
BCLC staging (0-B:C-D)
10:17
CNLC Staging (Ia-IIa:IIb-IIIa)
18:9
AFP (ng/mL)
249.00 (3.56-2287.42)
ALT (U/L)
31.48 ± 22.39
AST (U/L)
37.44 ± 26.24
TBIL
16.31 ± 9.37
DBIL
5.62 ± 4.15
IBIL
10.68 ± 6.53
Prothrombin time (second)
13.55 ± 2.35
Albumin
36.88 ± 5.36
Hemoglobin
135.11 ± 13.37
White blood cell count (/L)
4.84 ± 1.66
Platelet count (/L)
127.11 ± 91.61
Tumor maximum diameter (mm)
46 (15-130)
Tumor solitary:multiple
10:17
Hepatic encephalopathy (n)
0
Ascites, n (%)
11 (40.7)
Intraoperative blood loss (50-200:300-500)
19: 8
Hepatic artery embolization, n (%)
12 (44.4)
Postoperative recurrence and retreatment, n (%)
12 (44.4)
Postoperative MVI
8 (29.6)
Tumor capsule, n (%)
12 (44.4)
PDL1 positive, n (%)
17 (63.0)
Table 2 Clinical data for patients in the nonsurgical group.
Indicator
n = 29
Age (years)
60.38 ± 7.49
Gender (Male:female)
23:6
HIV initial diagnosis, n (%)
17 (58.6)
HIV-RNA positive, n (%)
20 (69.0)
MSM, n (%)
14 (48.3)
Received HART after HIV diagnosis
12 (41.4)
HBV, n (%)
21 (72.4)
HCV, n (%)
4 (13.8)
Chronic alcohol consumption, n (%)
11 (37.9)
CD4+ cell count < 200 (cell/μL)
18 (62.1)
Child-Pugh score (A:B)
14:15
BCLC staging (0-B:C-D)
12:17
CNLC Staging (Ia-IIa:IIb-IIIa)
14:15
AFP (ng/mL)
179.01 (1.64-848.74)
ALT (U/L)
23.66 ± 17.51
AST (U/L)
29.00 ± 20.56
TBIL
14.98 ± 6.82
DBIL
4.29 ± 2.49
IBIL
10.96 ± 4.86
Prothrombin time (second)
13.82 ± 2.11
Albumin
34.37 ± 5.43
Hemoglobin
129.55 ± 14.46
White blood cell count (/L)
5.41 ± 3.95
Platelet count (/L)
168.14 ± 73.22
Tumor maximum diameter (mm)
37 (9-115)
Tumor solitary:multiple
13:16
Hepatic encephalopathy (n)
0
Ascites, n (%)
7 (24.1)
PS score (0-1:2-3, cases)
19:10
SPSS 27.0 was used for the statistical analysis. Quantitative data are expressed as (mean ± SD) for normally distributed data and as medians for nonnormally distributed data. Qualitative data are presented as percentages. Group comparisons were performed using the Mann-Whitney U test, t test, and χ2 test to explore differences in survival prognosis and baseline data between the surgery and nonsurgery groups. Kaplan-Meier survival analysis was employed for disease-free survival (DFS) and overall survival (OS), and univariate and multivariate Cox regression analyses were conducted to identify factors influencing patient DFS and OS. A significance level of P < 0.05 was considered to indicate statistical significance.
RESULTS
Comparison of survival prognosis and baseline data between the surgery and nonsurgery groups
Intergroup analysis revealed significant differences in survival prognosis and baseline data between the surgery and nonsurgery groups. The median OS was 17 months in the surgery group, approximately 5 months longer than that in the nonsurgery group (P < 0.01) as illustrated in Figure 2. Significant differences were observed between the surgery and nonsurgery groups in terms of initial HIV diagnosis, Child-Pugh score, alpha-fetoprotein (AFP) measurement values, and initiation of HART therapy after an HIV diagnosis (P < 0.05; Table 3).
Figure 2 Differences in survival and prognosis between the surgical group and nonsurgical group.
HCC: Hepatocellular carcinoma; HIV: Human immunodeficiency virus; OS: Overall survival.
Table 3 Comparison of clinical parameters between the surgery and non-surgery groups.
Clinical parameters
Surgery group
Non-surgery group
P value
Age (years)
60.15 ± 5.90
60.38 ± 7.49
0.223
Gender (male:female)
24:3
23:6
0.472
HBV (positive:negative)
6:21
8:21
0.643
HCV (positive:negative)
2:25
4:25
0.440
CD4+ cell count < 200 (cell/μL)
15 (55.6)
18 (62.1)
0.621
HIV initial diagnosis, n (%)
20 (69.0)
17 (58.6)
0.222
HIV-RNA positive, n (%)
13 (48.1)
20 (69.0)
0.114
Initiation of HART therapy after HIV diagnosis, n (%)
Among the HIV-HCC patients who underwent liver resection (surgery group) 21 died by the end of follow-up (77.8%) with a median OS time of 17 months. The 6-month, 1-year, and 2-year OS rates were 88.9%, 61.6%, and 16.8%, respectively. Among patients with BCLC stage C-D disease (n = 17) the median OS time was 12 months with 6-month and 1-year OS rates of 89.2% and 36.7%, respectively.
Among HIV-HCC patients who did not undergo liver resection (nonsurgery group), 20 died (69.0%) with a median OS time of 12 months. The 6-month and 1-year OS rates were 82.4% and 42.3%, respectively. Among patients with BCLC stage C-D disease (n = 17) the median OS time was 9 months with 6-month and 1-year OS rates of 81.6% and 27.9%, respectively.
There were 21 patients who experienced recurrence by the end of follow-up (77.7%) in the surgery group, with a median DFS time of 13 months. The 6-month, 1-year, and 2-year DFS rates were 80.4%, 44.7%, and 22.3%, respectively (Figure 3).
Figure 3 Overall survival (human immunodeficiency virus) survival analysis of patients in the hepatocellular carcinoma-human immunodeficiency virus surgery group.
HIV: Human immunodeficiency virus; HCC: Hepatocellular carcinoma; OS: Overall survival; DFS: Disease-free survival.
Factors influencing patient OS and DFS
Univariate Cox regression analysis: For patients in the surgery group the risk factors influencing OS were men who have sex with men (MSM) status, advanced BCLC stage, postoperative MVI, and CD4+ T-cell count (cell/mL; all P < 0.05). The risk factors influencing DFS for HIV-HCC patients in the surgery group were MSM status, initial HIV diagnosis, CD4+ T-cell count < 200 (cell/μL), and advanced BCLC stage (all P < 0.05). Multivariate Cox regression analysis: A multivariate Cox regression analysis revealed that a CD4+ T-cell count < 200 (cell/μL) and MSM status (all P < 0.05) were significant risk factors affecting OS in HIV-HCC patients in the surgery group.
For detailed analysis and visualization, refer to Table 4, Table 5, Table 6, Table 7, Figure 4, and Figure 5.
Figure 4 Factors influencing patient overall survival (human immunodeficiency virus).
HIV: Human immunodeficiency virus; HCC: Hepatocellular carcinoma; MSM: Men who have sex with men; MVI: Microvascular invasion; OS: Overall survival.
Figure 5 Factors influencing patient disease-free survival.
HIV: Human immunodeficiency virus; HCC: Hepatocellular carcinoma; MSM: Men who have sex with men; MVI: Microvascular invasion; DFS: Disease-free survival.
Table 4 Single-factor Cox regression analysis of factors influencing overall survival in the surgical group.
Liver cancer is the fourth most prevalent and second most deadly cancer in China[11]. In 2020, there were approximately 410000 newly diagnosed cases of liver cancer in China, accounting for 45.3% of new cases worldwide[12]. Most liver HCC cases in China, a major country with HBV infection, evolve from HBV-related liver cirrhosis[13]. Surgery remains the most effective treatment for HCC[14,15]. Among these patients, those with HIV coinfection constitute a special group. With the increasing effectiveness of HAART the survival time of these patients has increased. However, liver disease is becoming a leading cause of death among people living with HIV[16,17], with HCC seemingly accounting for an increasing proportion of deaths[18].
Currently available literature is predominantly based on foreign data, with most studies being case reports or single-center results with small sample sizes. The literature indicates that HIV-positive patients with viral hepatitis are more prone to developing liver cirrhosis and early-onset liver cancer and exhibit greater tumor invasiveness[19]. This multicenter large-sample retrospective study involved four centers in Italy and included 588 HCC patients, 104 of whom were HIV-positive (17.7%)[20]. The study yielded several significant findings: (1) HIV-HCC patients were mostly male, relatively younger, and had earlier BCLC stages; (2) HIV-infected patients had significantly shorter HCC survival times, with median OS times of 35 months and 59 months, respectively (P = 0.048); (3) HIV-positive patients were more willing to undergo radical treatment than were HIV-negative patients and the prognoses of both groups undergoing radical treatment (surgery, radiofrequency ablation, or TNF-alpha converting enzyme combined with radiofrequency ablation) did not differ significantly, with median OS times of 52 months and 62 months, respectively (P = 0.901); and (4) In addition to well-known oncological characteristics, HIV RNA positivity was identified as an independent adverse prognostic factor for OS. Most of the data were based on patients with viral hepatitis, predominantly hepatitis C[21], which differs from the hepatitis B cases predominant in China[13,22]. Therefore, there is a need to explore HIV-HCC-related clinical data that align with our national context. According to long-term follow-up results from our center the main hepatitis type for Chinese HIV-HCC patients is hepatitis B (73.7%). The patients were mostly middle-aged to elderly men and the tumor staging distribution was similar to that of foreign data. However, the survival of patients who underwent radical treatment in our study was shorter than that reported in foreign studies (17 vs 52) possibly due to older age, poorer baseline conditions, and patient compliance with ART. We also report the occurrence of MVI after surgery, with a lower incidence rate (29.6%) than that reported by pathology experts in China (69.2%)[23]. Overall, the OS of the surgical group was shorter than that reported in the literature for surgical patients but a trend toward better prognosis with earlier staging was also demonstrated. Some foreign literature suggests that CD4+ T-cell counts are a prognostic factor[24,25] and our study provides similar statistically positive conclusions. Additionally, we found statistically significant differences (P < 0.05) in factors such as initial HIV diagnosis, MSM, microvascular invasion (MVI) postoperatively, and late-stage BCLC status.
We found that compared with patients in the nonsurgical group HIV-HCC patients who underwent surgical treatment had significantly longer survival (P < 0.05). Moreover, we identified factors influencing the prognosis of such patients, primarily the initial HIV diagnosis, CNLC stage, postoperative MVI on follow-up, and CD4+ T-cell count. Effective ART treatment for these patients can increase the CD4+ T-cell count, reduce the HIV RNA viral load, and decrease viral transmission[26,27], thereby improving the safety of surgery including health care worker safety. Hence, for patients without surgical contraindications the viral load or CD4+ count remains a factor of concern. Our study shows that HIV-positive patients with HCC experienced significantly prolonged survival after surgical treatment. Therefore, radical treatment should not be easily abandoned and regular follow-up and active postrecurrence treatment can achieve a better long-term prognosis.
HIV infection significantly impacts treatment strategies for HCC. When formulating treatment plans, health care workers must consider the complexity of the immune status of HIV-infected patients and potential drug interactions resulting from ART[28-30]. For HIV-positive HCC patients, HIV infection itself may affect tumor biology and patient response to treatment, thereby influencing the disease cure rate, recurrence rate, and long-term survival rate[31]. Hence, health care workers treating HIV-HCC patients must collaborate across disciplines to thoroughly understand the patient's overall condition and develop comprehensive, personalized treatment plans to control HIV infection effectively, treat HCC, and optimize patient quality of life.
This study has several limitations: It is retrospective and is a single-center study, limiting the level of evidence in evidence-based medicine. The sample size is relatively small and the time span is long. Due to the propensity for these patients to be overlooked, especially given the low proportion of patients undergoing treatment, particularly surgical resection, some results, trended but did not significantly differ. Therefore, in the next phase we will expand the sample size, conduct multicenter studies where feasible, and compare our findings with studies of HIV-negative patients to obtain more reliable conclusions.
CONCLUSION
Hepatectomy can effectively prolong the survival of patients with HIV-HCC but MVI identified during postoperative pathological examination, late tumor detection, late BCLC stage, CD4+ T < 200/μL and MSM are risk factors affecting the survival and prognosis of patients undergoing hepatectomy. In addition, there were significant differences between the surgical group and the nonsurgical group in terms of the initial diagnosis of HIV, Child-Pugh score, AFP measurement value, and HART-efficient ART after the diagnosis of HIV (P < 0.05). Therefore, these factors may also affect the survival and prognosis of patients.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Oncology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade A
Novelty: Grade A
Creativity or Innovation: Grade A
Scientific Significance: Grade A
P-Reviewer: Mulita F S-Editor: Lin C L-Editor: A P-Editor: Zhao S
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