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Article(id=1200026650403505001, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1200026645001241395, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2380.2023.0601, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1668009600000, receivedDateStr=2022-11-10, revisedDate=null, revisedDateStr=null, acceptedDate=1680192000000, acceptedDateStr=2023-03-31, onlineDate=1764038248873, onlineDateStr=2025-11-25, pubDate=1693152000000, pubDateStr=2023-08-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1764038248873, onlineIssueDateStr=2025-11-25, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1764038248873, creator=13701087609, updateTime=1764038248873, updator=13701087609, issue=Issue{id=1200026645001241395, tenantId=1146029695717560320, journalId=1189873630562394117, year='2023', volume='48', issue='8', pageStart='871', pageEnd='992', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1764038247584, creator=13701087609, updateTime=1764038741950, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1200028718564474883, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1200026645001241395, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1200028718564474884, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1200026645001241395, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=936, endPage=943, ext={EN=ArticleExt(id=1200026650843906938, articleId=1200026650403505001, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Characteristics and clinical significance of reactive oxygen species production by neutrophils in patients with chronic hepatitis B virus infection, columnId=1190310109000602400, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Clinical Research, runingTitle=null, highlight=null, articleAbstract=

Objective To analyze the level of reactive oxygen species (ROS) produced by neutrophils and to explore its clinical significance in patients with chronic hepatitis B virus (HBV) infection. Methods Eighty-eight chronic HBV infected patients who admitted to the Fifth Medical Center of Chinese PLA General Hospital from April 2022 to September 2022 were enrolled in this study. Thirty patients who received nucleoside (acid) analogues (NAs) treatment were classified as the treated group, and fifty-eight did not receive treatment were classified as the untreated group. Simultaneously, twenty healthy individuals were classified as control group. The differences in clinical and virological parameters were compared between the three groups. The spontaneous ROS production by neutrophils after incubation with DHR 123 fluorescent dye were detected by flow cytometry. And the correlation between the spontaneous ROS and HBV DNA viral load, hepatitis B surface antigen (HBsAg), white blood cell (WBC), C-reactive protein (CRP), alanine transaminase (ALT) and aspartate transaminase (AST) were further analyzed. Culture medium, HepG2 cell supernatant and HepG2.2.15 cell supernatant were used to co-culture with neutrophils from healthy controls, respectively, to verify the effect of HBV virus particles and proteins on neutrophil spontaneous ROS in vitro. The secondary ROS production by neutrophils after lipopolysaccharide (LPS) stimulation was compared between the three groups. Results The spontaneous ROS production by neutrophils in the untreated group was higher than control group (P<0.05). The spontaneous ROS production by neutrophils in untreated patients was positively correlated with HBV DNA viral load and HBsAg quantification (r=0.315, P=0.016; r=0.326, P=0.013), but had no significant correlation with WBC, CRP, ALT and AST. HepG2.2.15 cell supernatant could induce the spontaneous ROS production by neutrophils in a dose-dependent manner (P<0.05). After LPS stimulation, the secondary ROS production by neutrophils in the untreated group and the treated group were lower than the control group (P<0.05). Conclusion Reducing the viral load by antiviral treatment contributes to reduction of spontaneous ROS production by neutrophils but not to restore the secondary ROS production by neutrophils after stimulated by LPS.

, correspAuthors=Ruo-Nan Xu, Fu-Sheng Wang, authorNote=null, correspAuthorsNote=
Wang Fu-Sheng, E-mail:
Xu Ruo-Nan, E-mail:
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目的 分析慢性乙型肝炎病毒(HBV)感染患者中性粒细胞活性氧(ROS)的生成特点并探讨其临床意义。方法 选取2022年4-9月解放军总医院第五医学中心收治的88例慢性HBV感染者，其中58例未接受抗病毒治疗者纳入未治疗组，30例已进行核苷(酸)类似物(NAs)治疗者纳入治疗组，同时选取20名健康人作为对照组，比较各组临床指标及病毒学指标的差异。采用二氢罗丹明123(DHR 123)荧光染料与中性粒细胞进行孵育，通过流式细胞仪检测各组中性粒细胞自发ROS生成水平，并分析其与HBV DNA载量、乙肝表面抗原(HBsAg)定量、白细胞计数(WBC)、C反应蛋白(CRP)、谷丙转氨酶(ALT)及谷草转氨酶(AST)的相关性。分别使用完全培养基、HepG2细胞上清液及HepG2.2.15细胞上清液与健康人中性粒细胞共孵育，体外验证HBV病毒颗粒及蛋白对中性粒细胞自发ROS生成水平的影响。比较脂多糖(LPS)刺激后各组中性粒细胞继发ROS的生成水平。结果 与对照组比较，未治疗组患者中性粒细胞自发ROS生成水平增高(P<0.05)，且与HBV DNA载量、HBsAg定量呈正相关(r=0.315，P=0.016；r=0.326，P=0.013)，但与WBC、CRP、ALT及AST无明显相关性(P>0.05)。HepG2.2.15上清液可诱导中性粒细胞自发ROS生成水平增高(P<0.05)。LPS刺激后，未治疗组及治疗组患者中性粒细胞继发ROS生成水平均较对照组降低(P<0.05)。结论 HBV抗病毒治疗在降低病毒载量的同时可降低患者中性粒细胞自发ROS生成水平，但不能有效恢复LPS刺激后中性粒细胞继发ROS的生成能力。

, correspAuthors=徐若男, 王福生, authorNote=null, correspAuthorsNote=
王福生，E-mail：
徐若男，E-mail：
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冯芷倩，硕士研究生，主要从事病毒性肝炎的临床免疫学研究

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2解放军总医院第五医学中心感染病医学部/国家感染性疾病临床医学研究中心，北京 100039, bio={"content":"

冯芷倩，硕士研究生，主要从事病毒性肝炎的临床免疫学研究

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冯芷倩，硕士研究生，主要从事病毒性肝炎的临床免疫学研究

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figureFileBig=myxY6z6uVxJtg9jMX5CkAQ==, tableContent=null), ArticleFig(id=1200074165425373516, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=CN, label=图1, caption=外周血中性粒细胞自发ROS生成水平流式分析结果

ROS. 活性氧；MFI. 平均荧光强度；FMO. 荧光减一对照；A. 中性粒细胞流式圈门策略图；B. 组间外周血中性粒细胞自发ROS生成水平典型图；C. 组间外周血中性粒细胞自发ROS生成水平比较；D. 未治疗组依据HBV DNA载量分层后组间外周血中性粒细胞自发ROS生成水平比较；E. 未治疗组依据HBsAg定量水平分层后组间外周血中性粒细胞自发ROS生成水平比较；与对照组比较，(1)P<0.05；与HBV DNA<3.3 log10 IU/ml组比较，(2)P<0.01；与治疗组比较，(3)P<0.05

, figureFileSmall=naKqjrJQlWjeXsFAkLIfgg==, figureFileBig=myxY6z6uVxJtg9jMX5CkAQ==, tableContent=null), ArticleFig(id=1200074165559591248, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=EN, label=Fig.2, caption=Correlation analysis between the spontaneous ROS production levels of neutrophils and clinical indicators in patients with chronic HBV infection without treatment, figureFileSmall=306Ub49D5ctKit2EOXKc0w==, figureFileBig=E9sL3cOy9NsAGgrQQT25nQ==, tableContent=null), ArticleFig(id=1200074165656060243, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=CN, label=图2, caption=慢性HBV感染未治疗组患者中性粒细胞自发ROS生成水平与临床指标的相关性分析

HBV. 乙型肝炎病毒；HBsAg. 乙肝表面抗原；ALT. 谷丙转氨酶；AST. 谷草转氨酶；WBC. 白细胞计数；CRP. C反应蛋白

, figureFileSmall=306Ub49D5ctKit2EOXKc0w==, figureFileBig=E9sL3cOy9NsAGgrQQT25nQ==, tableContent=null), ArticleFig(id=1200074165760917846, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=EN, label=Fig. 3, caption=Flow cytometry analysis of the effect of HepG2.2.15 cell supernatant on the spontaneous ROS production level of neutrophils, figureFileSmall=wjfLAeAnLPnZdFGR54oNpA==, figureFileBig=o3pV1JgNePQZ76LioCy5Yg==, tableContent=null), ArticleFig(id=1200074165861581145, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=CN, label=图3, caption=HepG2.2.15细胞上清液影响中性粒细胞自发ROS生成水平流式分析

ROS. 活性氧；MFI. 平均荧光强度；FMO. 荧光减一对照；A. 纯化中性粒细胞流式圈门策略图；B. 中性粒细胞与不同浓度HepG2.2.15细胞上清液孵育后自发ROS生成水平典型图；C. 不同浓度HepG2.2.15及HepG2细胞上清液与中性粒细胞共孵育后自发ROS生成水平比较；与完全培养基(0%HepG2.2.15上清液组)比较，(1)P<0.05；与25%浓度的HepG2细胞上清液组比较，(2)P<0.01；与50%浓度的HepG2细胞上清液组比较，(3)P<0.01

, figureFileSmall=wjfLAeAnLPnZdFGR54oNpA==, figureFileBig=o3pV1JgNePQZ76LioCy5Yg==, tableContent=null), ArticleFig(id=1200074165941272924, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=EN, label=Fig.4, caption=Comparison of ROS production levels in peripheral blood neutrophils among groups after LPS stimulation, figureFileSmall=XHK/WwsPOBCkGs//mmy5rA==, figureFileBig=47pPwhc+lJGtigmKuzL/dQ==, tableContent=null), ArticleFig(id=1200074166054519135, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=CN, label=图4, caption=LPS刺激后各组外周血中性粒细胞ROS生成水平比较

ROS. 活性氧；MFI. 平均荧光强度；FMO. 荧光减一对照；A. LPS刺激后各组间中性粒细胞继发ROS生成水平典型图；B. LPS刺激后组间外周血中性粒细胞继发ROS生成水平比较；与对照组比较，(1)P<0.05

, figureFileSmall=XHK/WwsPOBCkGs//mmy5rA==, figureFileBig=47pPwhc+lJGtigmKuzL/dQ==, tableContent=null), ArticleFig(id=1200074166142599522, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=EN, label=Tab.1, caption=

Comparison of general information among each group of the enrolled patients

, figureFileSmall=null, figureFileBig=null, tableContent=
项目对照组(n=20)未治疗组(n=58)治疗组(n=30)Z/F/χ2P
性别(男/女, 例)6/1436/2210/200.4730.791
年龄(岁, $\bar{x}±s$)35.7±8.238.5±10.841.9±12.12.1300.124
WBC(×109/L, $\bar{x}±s$)5.49±0.925.52±1.284.95±1.432.1990.116
ALT[U/L, M(Q1, Q3)]18.0(14.3, 26.0)42.0(21.8, 258.3)(1)22.0(12.8, 34.6)(2)21.516<0.001
AST[U/L, M(Q1, Q3)]21.5(16.5, 29.0)31.5(23.0, 89.0)(1)23.0(19.0, 28.5)(2)17.290<0.001
HBV DNA载量[(log10 IU/ml, M(Q1, Q3)]-4.45(2.31, 7.79)1.60(1.30, 2.17)2.769<0.001
HBsAg定量 [(log10 IU/ml, M(Q1, Q3)]-3.71(2.84, 4.57)3.00(2.63, 3.52)5.9130.005
), ArticleFig(id=1200074166243262820, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1200026650403505001, language=CN, label=表1, caption=

各组一般资料比较

, figureFileSmall=null, figureFileBig=null, tableContent=
项目对照组(n=20)未治疗组(n=58)治疗组(n=30)Z/F/χ2P
性别(男/女, 例)6/1436/2210/200.4730.791
年龄(岁, $\bar{x}±s$)35.7±8.238.5±10.841.9±12.12.1300.124
WBC(×109/L, $\bar{x}±s$)5.49±0.925.52±1.284.95±1.432.1990.116
ALT[U/L, M(Q1, Q3)]18.0(14.3, 26.0)42.0(21.8, 258.3)(1)22.0(12.8, 34.6)(2)21.516<0.001
AST[U/L, M(Q1, Q3)]21.5(16.5, 29.0)31.5(23.0, 89.0)(1)23.0(19.0, 28.5)(2)17.290<0.001
HBV DNA载量[(log10 IU/ml, M(Q1, Q3)]-4.45(2.31, 7.79)1.60(1.30, 2.17)2.769<0.001
HBsAg定量 [(log10 IU/ml, M(Q1, Q3)]-3.71(2.84, 4.57)3.00(2.63, 3.52)5.9130.005
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慢性乙型肝炎病毒感染患者中性粒细胞活性氧的生成特点及临床意义
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冯芷倩 1, 2 , 鲍春梅 3 , 汪海燕 2, 4 , 杨涛 2 , 唐莉莉 2 , 徐若男 1, 2, * , 王福生 1, 2, *
解放军医学杂志 | 临床研究 2023,48(8): 936-943
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解放军医学杂志 | 临床研究 2023, 48(8): 936-943
慢性乙型肝炎病毒感染患者中性粒细胞活性氧的生成特点及临床意义
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冯芷倩1, 2, 鲍春梅3, 汪海燕2, 4, 杨涛2, 唐莉莉2, 徐若男1, 2, * , 王福生1, 2, *
作者信息
  • 1南方医科大学第二临床医学院，广东广州 510515
  • 2解放军总医院第五医学中心感染病医学部/国家感染性疾病临床医学研究中心，北京 100039
  • 3解放军总医院第五医学中心检验科，北京 100039
  • 4中国科学技术大学生命科学与医学部附属第一医院，安徽合肥 230001

    • 冯芷倩，硕士研究生，主要从事病毒性肝炎的临床免疫学研究

通讯作者:

王福生，E-mail：
徐若男，E-mail：
Characteristics and clinical significance of reactive oxygen species production by neutrophils in patients with chronic hepatitis B virus infection
Zhi-Qian Feng1, 2, Chun-Mei Bao3, Hai-Yan Wang2, 4, Tao Yang2, Li-Li Tang2, Ruo-Nan Xu1, 2, * , Fu-Sheng Wang1, 2, *
Affiliations
  • 1The Second School of Clinical Medicine, Southern Medical University, Guangzhou, Guangdong 510515, China
  • 2Senior Department of Infectious Diseases/National Clinical Research Center for Infectious Diseases, the Fifth Medical Center of Chinese PLA General Hospital, Beijing 100039, China
  • 3Clinical Laboratory, the Fifth Medical Center of Chinese PLA General Hospital, Beijing 100039, China
  • 4The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui 230001, China
出版时间: 2023-08-28 doi: 10.11855/j.issn.0577-7402.2380.2023.0601
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摘要
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目的 分析慢性乙型肝炎病毒(HBV)感染患者中性粒细胞活性氧(ROS)的生成特点并探讨其临床意义。方法 选取2022年4-9月解放军总医院第五医学中心收治的88例慢性HBV感染者，其中58例未接受抗病毒治疗者纳入未治疗组，30例已进行核苷(酸)类似物(NAs)治疗者纳入治疗组，同时选取20名健康人作为对照组，比较各组临床指标及病毒学指标的差异。采用二氢罗丹明123(DHR 123)荧光染料与中性粒细胞进行孵育，通过流式细胞仪检测各组中性粒细胞自发ROS生成水平，并分析其与HBV DNA载量、乙肝表面抗原(HBsAg)定量、白细胞计数(WBC)、C反应蛋白(CRP)、谷丙转氨酶(ALT)及谷草转氨酶(AST)的相关性。分别使用完全培养基、HepG2细胞上清液及HepG2.2.15细胞上清液与健康人中性粒细胞共孵育，体外验证HBV病毒颗粒及蛋白对中性粒细胞自发ROS生成水平的影响。比较脂多糖(LPS)刺激后各组中性粒细胞继发ROS的生成水平。结果 与对照组比较，未治疗组患者中性粒细胞自发ROS生成水平增高(P<0.05)，且与HBV DNA载量、HBsAg定量呈正相关(r=0.315，P=0.016；r=0.326，P=0.013)，但与WBC、CRP、ALT及AST无明显相关性(P>0.05)。HepG2.2.15上清液可诱导中性粒细胞自发ROS生成水平增高(P<0.05)。LPS刺激后，未治疗组及治疗组患者中性粒细胞继发ROS生成水平均较对照组降低(P<0.05)。结论 HBV抗病毒治疗在降低病毒载量的同时可降低患者中性粒细胞自发ROS生成水平，但不能有效恢复LPS刺激后中性粒细胞继发ROS的生成能力。

乙型肝炎病毒  /  抗病毒治疗  /  活性氧  /  中性粒细胞

Objective To analyze the level of reactive oxygen species (ROS) produced by neutrophils and to explore its clinical significance in patients with chronic hepatitis B virus (HBV) infection. Methods Eighty-eight chronic HBV infected patients who admitted to the Fifth Medical Center of Chinese PLA General Hospital from April 2022 to September 2022 were enrolled in this study. Thirty patients who received nucleoside (acid) analogues (NAs) treatment were classified as the treated group, and fifty-eight did not receive treatment were classified as the untreated group. Simultaneously, twenty healthy individuals were classified as control group. The differences in clinical and virological parameters were compared between the three groups. The spontaneous ROS production by neutrophils after incubation with DHR 123 fluorescent dye were detected by flow cytometry. And the correlation between the spontaneous ROS and HBV DNA viral load, hepatitis B surface antigen (HBsAg), white blood cell (WBC), C-reactive protein (CRP), alanine transaminase (ALT) and aspartate transaminase (AST) were further analyzed. Culture medium, HepG2 cell supernatant and HepG2.2.15 cell supernatant were used to co-culture with neutrophils from healthy controls, respectively, to verify the effect of HBV virus particles and proteins on neutrophil spontaneous ROS in vitro. The secondary ROS production by neutrophils after lipopolysaccharide (LPS) stimulation was compared between the three groups. Results The spontaneous ROS production by neutrophils in the untreated group was higher than control group (P<0.05). The spontaneous ROS production by neutrophils in untreated patients was positively correlated with HBV DNA viral load and HBsAg quantification (r=0.315, P=0.016; r=0.326, P=0.013), but had no significant correlation with WBC, CRP, ALT and AST. HepG2.2.15 cell supernatant could induce the spontaneous ROS production by neutrophils in a dose-dependent manner (P<0.05). After LPS stimulation, the secondary ROS production by neutrophils in the untreated group and the treated group were lower than the control group (P<0.05). Conclusion Reducing the viral load by antiviral treatment contributes to reduction of spontaneous ROS production by neutrophils but not to restore the secondary ROS production by neutrophils after stimulated by LPS.

hepatitis B virus  /  antiviral treatment  /  reactive oxygen species  /  neutrophils
冯芷倩, 鲍春梅, 汪海燕, 杨涛, 唐莉莉, 徐若男, 王福生. 慢性乙型肝炎病毒感染患者中性粒细胞活性氧的生成特点及临床意义. 解放军医学杂志, 2023 , 48 (8) : 936 -943 . DOI: 10.11855/j.issn.0577-7402.2380.2023.0601
Zhi-Qian Feng, Chun-Mei Bao, Hai-Yan Wang, Tao Yang, Li-Li Tang, Ruo-Nan Xu, Fu-Sheng Wang. Characteristics and clinical significance of reactive oxygen species production by neutrophils in patients with chronic hepatitis B virus infection[J]. Medical Journal of Chinese People’s Liberation Army, 2023 , 48 (8) : 936 -943 . DOI: 10.11855/j.issn.0577-7402.2380.2023.0601
正文
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乙型肝炎病毒(hepatitis B virus，HBV)是一类嗜肝DNA病毒，慢性HBV感染可引起广泛的肝脏疾病，增加患者进展为肝硬化、肝癌的风险[1-2]。目前，慢性HBV感染仍是全球重大的公共卫生问题之一，我国现存HBV携带者数量超过9700万[3-4]。天然免疫细胞在HBV病毒学控制、病毒抗原递呈、肝细胞特异/非特异损伤及修复过程中发挥着重要作用[5-7]。中性粒细胞是免疫系统中占比最大的细胞群体，具有强大的抗感染及免疫调节潜能。近年来，越来越多的研究证实中性粒细胞在病毒性疾病发病机制中发挥着重要作用[8-9]。人类免疫缺陷病毒(human immunodeficiency virus，HIV)感染过程中，中性粒细胞是保护机体抵抗HIV感染及控制病毒传播的重要介质，中性粒细胞功能紊乱与感染风险增高、T细胞免疫耗竭、炎性损伤增加等环节密切相关[10]。但在HBV感染过程中，中性粒细胞功能变化与HBV病毒学应答之间的关系尚未完全阐明。
中性粒细胞肝内大量浸润、功能失衡可能是导致肝细胞损伤及HBV病毒持续复制的重要原因[11]。各类细胞因子、活性氧(reactive oxygen species，ROS)等是中性粒细胞发挥功能的主要效应分子。尽管中性粒细胞的激活有利于抗病毒免疫，但其不当和(或)长期激活可对宿主产生不利影响[12]。ROS既是信号分子，也是炎症反应的中介物，而中性粒细胞是ROS产生的主要来源[12]。目前关于慢性乙肝发病过程中中性粒细胞ROS产生特点的研究较少。本研究检测慢性HBV感染患者外周血中性粒细胞ROS的生成水平，分析ROS水平与HBV相关临床指标的关系，并探讨了影响中性粒细胞ROS分泌的可能原因。
1 资料与方法
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1.1 一般资料
选取2022年4-9月在解放军总医院第五医学中心确诊为慢性HBV感染的患者88例，均符合《慢性乙型肝炎防治指南(2019年版)》中的诊断标准[13]。排除标准：(1)合并甲型肝炎病毒(hepatitis A virus，HAV)、丙型肝炎病毒(hepatitis C virus，HCV)、丁型肝炎病毒(hepatitis D virus，HDV)或HIV等病毒感染或细菌感染。(2)合并自身免疫性肝炎、酒精性肝炎、药物性肝炎，脂肪肝等非HBV病毒性肝炎。(3)伴有其他严重身心疾病、感染、既往有肝硬化病史或入组筛选行影像学检查时提示存在明确肝硬化。(4)合并发热。(5)既往有肿瘤疾病史。(6)妊娠女性、精神疾病患者，或研究者认为存在不适宜入组的其他情况。根据患者治疗情况，将其中58例未接受抗病毒治疗者归入未治疗组，30例接受6个月以上核苷(酸)类似物(NAs)抗病毒治疗者归入治疗组。另选取20名健康人作为对照组。本研究经解放军总医院第五医学中心伦理委员会批准(审批号：KY-2022-6-42-1)，所有入组对象均签署知情同意书。
1.2 方法
1.2.1 一般资料获取
通过查询病例资料，收集研究对象的性别、年龄、既往病史、化验检查结果[如肝功能、血常规、HBV DNA载量、乙肝表面抗原(HBsAg)定量]等临床资料。
1.2.2 流式细胞仪检测中性粒细胞ROS分泌功能
采集对照组以及未治疗组和治疗组患者肘静脉血10 ml于EDTA抗凝管中，检测外周血中性粒细胞自发及继发ROS水平。步骤如下：各取100 μl全血分别装入3支流式管中，置于冰水浴中10 min，充分冷却至0 ℃。其中一管加入0.2 μl二氢罗丹明123(dihydrorhodamine 123，DHR 123，美国AAT Bioquest公司)，混匀后于37 ℃孵育10 min；另一管不加DHR 123作为荧光减一对照(fluorescence minus one，FMO)；剩余一管加入100 ng/ml脂多糖(LPS)，涡旋混匀后立即置于37 ℃水浴锅中孵育10 min，再加入0.2 μl DHR 123，混匀后继续于37 ℃孵育10 min。加入磷酸盐缓冲液(PBS)洗涤，以1300 r/min离心5 min，弃上清，用PBS溶液100 µl重悬细胞。3管中均加入抗CD66b-PE-Cy7抗体(美国Biolegend公司)对全血进行表型染色，混合均匀后置于室温避光孵育30 min。加入2 ml溶血素，充分混匀后避光静置5 min，以1500 r/min离心5 min，弃上清后重悬细胞。加入1 ml PBS再次进行洗涤后，弃上清，重悬细胞，随后加入1%多聚甲醛300 μl固定。用FACSymphonyTM A5流式细胞仪检测中性粒细胞ROS产生的平均荧光强度(mean fluorescence intensity，MFI)，应用FlowJo软件分析流式细胞仪检测结果。
1.2.3 HepG2.2.15和HepG2细胞培养及上清液收集
HepG2.2.15及HepG2细胞均由解放军总医院第五医学中心提供，将此两种细胞接种于含10%胎牛血清+1%双抗的DMEM培养基，在25 cm2培养瓶中于37 ℃、5%CO2、95%湿度的恒温培养箱中培养，以胰蛋白酶消化后传代。培养3 d后，常温下以1000 r/min离心5 min，去除细胞杂质后，收集上清液备存。
1.2.4 中性粒细胞分离纯化
使用EDTA抗凝真空采血管无菌采集健康人外周静脉血10 ml，以2000 r/min离心10 min，去除上层血浆，取剩余血细胞，用等量PBS混悬，并用巴氏滴管轻柔吹吸。取15 ml离心管，底部加入Ficoll-Paque PLUS淋巴细胞分离液5 ml。用巴氏滴管吸取血细胞混合液后，缓慢平铺于淋巴分离液上层。配平后放入离心机中，以2500 r/min离心20 min。离心后的液体分为4层，留取粒细胞及红细胞层，用等量生理盐水混匀，加入1/3体积量的红细胞沉降液混匀并常温静置30 min。取静置后红细胞层分界线上层液体，加入生理盐水洗涤细胞，以1200 r/min离心5 min。中性粒细胞震荡后，加入0.2% NaCl溶液2 ml以裂解红细胞，30 s后加入1.6% NaCl溶液2 ml终止，另适量补充生理盐水洗涤细胞，以1200 r/min离心5 min后，弃上清，依据实验需要加入DMEM完全培养基，重悬细胞后，稀释计数，以备检测中性粒细胞自发ROS生成水平。
1.2.5 中性粒细胞自发ROS生成水平检测
吸取1.5×106/ml的纯化健康人中性粒细胞500 µl，均匀铺至24孔板内。将中性粒细胞分别与DMEM完全培养基，25%、50%浓度的HepG2及HepG2.2.15细胞上清液共孵育12 h。收集中性粒细胞，检测其自发ROS的生成水平。
1.3 统计学处理
采用GraphPad Prism 9.0软件进行统计分析并作图。符合正态分布的计量资料以$\bar{x}±s$表示，两组间比较采用t检验，多组比较采用方差分析。非正态分布计量资料以M(Q1，Q3)表示，两组间比较采用Mann-Whitney U检验，多组间比较采用Kruskal-Wallis检验。计数资料以例(%)表示，比较采用χ2检验，相关性分析采用Spearman检验。P<0.05为差异有统计学意义。
2 结果
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2.1 各组一般资料比较
各组性别、年龄及白细胞计数差异无统计学意义(P>0.05)。未治疗组ALT及AST均高于治疗组及对照组，差异有统计学意义(P<0.01)。未治疗组HBV DNA载量、HBsAg定量均高于治疗组，差异有统计学意义(P<0.01，表1)。
2.2 各组中性粒细胞自发ROS生成水平比较
未治疗组中性粒细胞自发ROS生成水平高于对照组(P<0.05)。对照组与治疗组间、未治疗组与治疗组间差异均无统计学意义(P>0.05，图1A、B、C)。HBV DNA载量≥3.3 log10 IU/ml患者的中性粒细胞自发ROS生成水平高于HBV DNA载量<3.3 log10 IU/ml的患者(P<0.01)，并明显高于治疗组及对照组(P<0.05，图1D)。HBsAg≥3 log10 IU/ml患者的中性粒细胞自发ROS生成水平明显高于治疗组及对照组(P<0.05，图1E)。
2.3 慢性HBV感染患者中性粒细胞自发ROS生成水
平与临床指标的关系HBV感染未治疗组患者中性粒细胞自发ROS生成水平与HBV DNA载量(r=0.315，P=0.016)及HBsAg定量水平(r=0.326，P=0.013)呈正相关，与ALT(r=0.097，P=0.469)、AST(r=0.128，P=0.338)、WBC(r=0.151，P=0.258)无相关性（图2）。未治疗组58例患者中共有18例进行了CRP检测，其CRP水平与中性粒细胞自发ROS生成水平无相关性(r=-0.222，P=0.377，图2)。HBV感染治疗组患者中性粒细胞自发ROS生成水平与HBV DNA载量、HBsAg定量水平、ALT、AST、WBC及CRP均无相关性(P>0.05)。
2.4 HepG2.2.15细胞上清液对中性粒细胞自发ROS生成水平的影响
与完全培养基孵育的中性粒细胞相比，包含HBV病毒的HepG2.2.15细胞上清液能明显上调中性粒细胞自发ROS的生成水平，且呈剂量依赖性(P<0.05)。而不同浓度HepG2细胞上清液孵育后中性粒细胞的自发ROS生成水平无明显变化(P>0.05)。同时，25%浓度的HepG2.2.15细胞上清液孵育后中性粒细胞自发ROS生成水平高于25%浓度的HepG2细胞上清液孵育(P<0.01)；50%浓度的HepG2.2.15细胞上清液孵育后中性粒细胞自发ROS生成水平高于50%浓度HepG2细胞上清液孵育(P<0.01，图3)。
2.5 LPS刺激后慢性HBV感染患者中性粒细胞继发ROS生成能力比较
慢性HBV感染患者治疗组及未治疗组的中性粒细胞经LPS刺激后，其继发ROS生成水平均较对照组下降，差异有统计学意义(P<0.05，图4)。未治疗组及治疗组患者中性粒细胞继发ROS生成水平与HBV DNA载量、HBsAg定量水平、WBC、CRP、ALT及AST均无相关性(P>0.05)。
3 讨论
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适应性免疫细胞在控制HBV感染中起着至关重要的作用，然而越来越多的研究证实天然免疫细胞能够感知HBV并对之产生应答。在HBV感染期间，适应性免疫的相关研究结果尚不能完全解释持续存在的HBV感染及肝脏免疫病理学损伤。有效、协调的天然和适应性免疫反应有助于机体清除HBV并促进宿主持久免疫的形成。对慢性HBV感染期间天然免疫的研究有助于进一步了解宿主复杂的免疫反应，并设计新的干预策略。
慢性HBV感染可改变机体肝脏及循环微环境，继而导致免疫细胞功能、表型的改变[6]。多种天然免疫细胞如巨噬细胞、单核细胞、自然杀伤(NK)细胞及树突状细胞的频率、功能及表型改变，与适应性免疫间的相互作用及对HBV控制的作用已被报道[14]。近年来的研究证实，中性粒细胞能够感知病毒并通过功能及表型的改变发挥抗病毒或促进病毒的双重作用[7]。此外，研究表明天然免疫细胞的活化与HBV感染患者肝损伤及纤维化严重程度呈正相关，且慢性乙型肝炎患者肝脏中性粒细胞浸润明显增加[11]，提示中性粒细胞活化可能会促进HBV感染患者肝脏免疫病理学进展。目前，中性粒细胞在HBV感染中表型及功能的变化特点尚未见详细报道。本研究通过流式细胞术检测慢性HBV感染患者中性粒细胞ROS的生成能力，结果表明，未进行抗病毒治疗的慢性HBV感染患者中性粒细胞存在基础性活化，其自发ROS生成能力增加。中性粒细胞通过生成ROS发挥抗菌及抗病毒作用，但不当的ROS生成又会加重组织损害[15-16]。ROS的过度蓄积可能是促进机体炎性反应、引起局部组织损伤的重要原因[12，16]。
丙型肝炎患者中性粒细胞存在功能障碍，抗病毒治疗有助于恢复其中性粒细胞功能[17]。本研究结果表明，未经抗病毒治疗的患者中性粒细胞自发ROS生成水平较对照组增高。进一步将未治疗组患者依据HBV DNA载量及HBsAg定量水平进行分层分析发现，HBV DNA≥3.3 log10 IU/ml及HBsAg≥3 log10 IU/ml者中性粒细胞自发ROS生成水平均明显升高，且中性粒细胞自发ROS生成能力与HBV DNA载量及HBsAg定量呈正相关。而在HBV DNA<3.3 log10 IU/ml、HBsAg<3 log10 IU/ml及接受抗病毒治疗的患者中，中性粒细胞自发ROS生成水平未明显升高，提示HBV的存在是中性粒细胞自发ROS生成活跃的重要原因。同时，未治疗组及治疗组患者中性粒细胞自发ROS生成水平与WBC、CRP无相关性，这可能与筛选患者时排除了炎症水平波动者有关。此外，无论是未治疗组还是治疗组患者，均未发现中性粒细胞自发ROS生成水平与肝脏炎症指标ALT、AST存在相关性，可能与外周血中性粒细胞功能不能完全反映肝脏内中性粒细胞功能有关，尚需进一步通过肝脏组织原位ROS检测进行验证。中性粒细胞自发ROS在HBV感染者体内的生成增加是有助于机体清除病毒还是介导肝脏的损伤及病理进展尚需进一步探究。本研究发现，未治疗组及治疗组患者中性粒细胞经LPS刺激后继发ROS生成水平均低于对照组，提示抗病毒治疗降低病毒的同时不能有效恢复中性粒细胞继发ROS的生成能力。此外，本研究发现未治疗组及治疗组患者中性粒细胞经LPS刺激后继发ROS生成水平与HBV DNA载量、HBsAg定量水平、WBC、CRP、ALT及AST不存在相关性。研究表明，HBeAg及HBcAg能够有效抑制中性粒细胞ROS的继发生成能力[18]，因此HBV感染者机体存在的HBeAg及HBcAg可能是影响中性粒细胞ROS继发生成能力的主要原因之一，具体机制仍需要深入探究。
HepG2.2.15细胞上清液含有HBV病毒颗粒及相关蛋白，本研究通过体外实验证实HepG2.2.15上清可明显提高中性粒细胞自发ROS生成水平，而不含HBV病毒颗粒及蛋白的HepG2上清无类似效应，提示HBV病毒颗粒及蛋白的存在可能影响中性粒细胞ROS的生成。慢性HBV感染患者中性粒细胞内存在HBV DNA的富集[19]，同时中性粒细胞表达多种模式识别受体(pattern-recognition receptors，PRRs)以识别病毒颗粒及蛋白，Toll样受体(Toll-like receptors，TLR)作为病毒感染过程中最为重要的一种PRRs，可感知HBeAg、HBcAg的刺激信息[5，20-21]，进而影响中性粒细胞趋化、ROS生成、细胞凋亡及中性粒细胞捕获网(neutrophil extracellular traps，NETs)的水平[18，22]。研究显示，中性粒细胞可表达除TLR3以外几乎所有的TLR，且TLR的激动与ROS的生成密切相关[23-25]。鉴于中性粒细胞本身的异质性及TLR表达的多样性，不同TLR感知HBV病毒颗粒及蛋白刺激的能力存在明显差异。例如，TLR-9可感知HBV病毒颗粒的刺激，TLR-2可明确感知e抗原的刺激。本研究存在一定局限性。例如，纳入患者中仅有部分进行了CRP检测，无法更好地阐明CRP与中性粒细胞自发ROS生成水平的相关性；此外，在HBV感染过程中，病毒颗粒及相关蛋白可能直接影响中性粒细胞ROS的生成，但本研究未进一步对病毒颗粒及HBV相关蛋白进行区分，以明确其对中性粒细胞自发及继发ROS生成能力的影响；且本研究为横断面研究，中性粒细胞ROS生成水平变化在HBV感染期间发挥的具体作用仍需通过建立纵向队列进一步深入探讨。
综上所述，病毒学阳性的慢性HBV感染患者中性粒细胞自发ROS生成水平升高，抗病毒治疗在降低病毒载量的同时，还能逆转中性粒细胞自发ROS生成，但不能有效恢复LPS刺激后中性粒细胞ROS的表达，提示中性粒细胞对抗病毒治疗存在应答响应，但其功能异常在HBV感染过程中仍持续存在。了解中性粒细胞与宿主免疫系统之间的关系，有助于进一步解析HBV感染的免疫学机制。
基金
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  • 国家自然科学基金(82171732)
  • 国家自然科学基金(81721002)
文献
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2023年第48卷第8期
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文章信息
doi: 10.11855/j.issn.0577-7402.2380.2023.0601
  • 接收时间：2022-11-10
  • 首发时间：2025-11-25
  • 出版时间：2023-08-28
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  • 收稿日期：2022-11-10
  • 录用日期：2023-03-31
基金
National Natural Science Foundation of China(82171732)
国家自然科学基金(82171732)
National Natural Science Foundation of China(81721002)
国家自然科学基金(81721002)
作者信息
    1南方医科大学第二临床医学院，广东广州 510515
    2解放军总医院第五医学中心感染病医学部/国家感染性疾病临床医学研究中心，北京 100039
    3解放军总医院第五医学中心检验科，北京 100039
    4中国科学技术大学生命科学与医学部附属第一医院，安徽合肥 230001

通讯作者:

王福生，E-mail：
徐若男，E-mail：
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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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