不同时段华支睾吸虫排泄分泌产物的免疫原性及其诊断价值

doi:10.12140/j.issn.1000-7423.2025.03.021

中国寄生虫学与寄生虫病杂志 ›› 2025, Vol. 43 ›› Issue (3): 440-445.doi: 10.12140/j.issn.1000-7423.2025.03.021

不同时段华支睾吸虫排泄分泌产物的免疫原性及其诊断价值

吴雨洪¹()(), 邓雪玲¹, 黄世圣², 吴美欣², 罗柳春³, 傅晓茵⁴^,⁵^,⁶, 战廷正⁴^,⁵^,⁶, 李青¹^,⁵^,⁶, 唐泽丽¹^,⁵^,⁶^,^*()()

1 广西医科大学基础医学院细胞生物学与遗传学教研室，广西南宁 530021
2 广西医科大学第一附属医院，广西南宁 530021
3 柳州市人民医院，广西柳州 545006
4 广西医科大学基础医学院寄生虫学教研室，广西南宁 530021
5 广西高校区域性疾病基础研究重点实验室，广西医科大学，广西南宁 530021
6 广西医科大学长寿与老年相关疾病教育部重点实验室，广西南宁 530021

收稿日期:2024-07-27 修回日期:2024-11-27 出版日期:2025-06-30 发布日期:2025-05-07
通讯作者: *唐泽丽（ORCID：0009-0007-7852-4129），女，博士，副教授，主要从事病原生物功能蛋白免疫学研究。E-mail：Tangzeli_team99@163.com
作者简介:吴雨洪（ORCID：0000-0002-2436-0655），女，硕士研究生，从事病原生物功能蛋白免疫学研究。E-mail：wyh6781226@163.com
基金资助:
国家自然科学基金(31900681);广西自然科学基金(2023GXNSFAA026201);广西自然科学基金(2018GXNSFBA050070);广西医科大学一流学科创新驱动人才计划

Immunogenicity of excretory/secretory products of Clonorchis sinensis at different stages and its diagnostic value for clonorchiasis

WU Yuhong¹()(), DENG Xueling¹, HUANG Shisheng², WU Meixin², LUO Liuchun³, FU Xiaoyin⁴^,⁵^,⁶, ZHAN Tingzheng⁴^,⁵^,⁶, LI Qing¹^,⁵^,⁶, TANG Zeli¹^,⁵^,⁶^,^*()()

1 Department of Cell Biology and Genetics, School of Basic Medical Sciences, Guangxi Medical University, Nanning 530021, Guangxi, China
2 The First Affiliated Hospital of Guangxi Medical University, Nanning 530021, Guangxi, China
3 Liuzhou People’s Hospital, Liuzhou 545006, Guangxi, China
4 Department of Parasitology, School of Basic Medical Sciences, Guangxi Medical University, Nanning 530021, Guangxi, China
5 Key Laboratory of Basic Research on Regional Diseases, Guangxi Medical University, Nanning 530021, Guangxi, China
6 Key Laboratory of Longevity and Aging-Related Diseases of Chinese Ministry of Education, Guangxi Medical University, Nanning 530021, Guangxi, China

Received:2024-07-27 Revised:2024-11-27 Online:2025-06-30 Published:2025-05-07
Contact: *E-mail: Tangzeli_team99@163.com
Supported by:
National Natural Science Foundation of China(31900681);Guangxi Natural Science Foundation(2023GXNSFAA026201);Guangxi Natural Science Foundation(2018GXNSFBA050070);Guangxi Medical University First-Class Discipline Innovation-Driven Talent Program

摘要/Abstract

摘要：

比较华支睾吸虫不同时段排泄/分泌产物（CsESP）的免疫原性，评估其用于诊断华支睾吸虫病的价值。体外培养华支睾吸虫成虫，分别收集培养0~24 h和24~48 h的培养液并混合，制备成CsESP-1和CsESP-2抗原。小鼠随机分为CsESP-1组、CsESP-2组、佐剂组和PBS组4组，使用对应的抗原进行皮下免疫，并于免疫第0、2、4、6周采集血液制备免疫血清，ELISA法检测免疫小鼠血清中CsESP抗体滴度和IgG、IgG1水平。以CsESP-1和CsESP-2抗原ELISA检测健康者（Cs^-）和华支睾吸虫感染者（Cs⁺）血样中CsESP特异性IgG及亚类水平，使用SPSS 27.0软件生成敏感度、特异度和约登指数，绘制受试者工作特征（ROC）曲线并计算ROC曲线下面积（AUC），根据AUC评价抗原的诊断效果。取Cs^-、Cs⁺、粪类圆线虫感染者、巨片形吸虫感染者和疟疾患者血样，ELISA检测交叉反应。两组比较采用t检验，AUC的比较采用配对ROC分析。ELISA结果显示，免疫第6周CsESP-1组和CsESP-2组小鼠血清的CsESP抗体滴度分别为1:102 400和1:400，CsESP-1的抗体滴度优于CsESP-2。CsESP-1组小鼠在免疫第6周的特异性IgG和IgG1 A₄₅₀值分别为0.926和1.803，均高于佐剂组的0.147和0.080（t = 5.805、5.643，均P < 0.05）。CsESP-2组小鼠在免疫第2、4、6周的特异性IgG A₄₅₀值分别为0.279、0.437、0.523，均高于佐剂组的0.133、0.127、0.142（t = 2.906、5.286、6.83，P < 0.05、0.05、0.01）；在第4、6周的IgG1 A₄₅₀值为0.225和0.332，均高于佐剂组的0.095和0.083（t = 3.423、2.485，均P < 0.05）。Cs⁺血样中CsESP-1特异性IgG、IgG2和IgG4的A₄₅₀值分别为0.817、0.274和0.524，均高于Cs^-血样的0.456、0.102和0.103（t = 7.184、2.720、5.634，均P < 0.01）；CsESP-2特异性IgG、IgG1、IgG2和IgG4的A₄₅₀值分别为0.783、0.132、0.233和0.465，均高于Cs^-血样的0.460、0.068、0.074和0.082（t = 4.768、2.519、2.634、4.991，P < 0.01、0.05、0.05、0.01）。CsESP-1抗原检测Cs⁺血样IgG4的综合效果最优，敏感度、特异度和准确度分别为89.2%、86.5%和87.9%；CsESP-2抗原检测Cs⁺血样IgG4的综合效果也最优，敏感度、特异度和准确度也分别为89.2%、86.5%和87.9%。ROC曲线显示，CsESP-1抗原检测IgG1和IgG2均具有一定的诊断价值（均AUC > 0.7），检测IgG和IgG4均具有较高的诊断价值（均AUC > 0.9）；CsESP-2抗原检测IgG、IgG1和IgG2均具有一定的诊断价值（均AUC > 0.7），检测IgG4具有较高的诊断价值（AUC > 0.9）。配对ROC分析显示，CsESP-1抗原对IgG和IgG1的诊断效能高于CsESP-2抗原（z = 3.515、2.149，P < 0.01、0.05）。CsESP-1和CsESP-2抗原与粪类圆线虫感染者、巨片形吸虫感染者和疟疾患者血样的IgG均无交叉反应。本研究制备的CsESP-1和CsESP-2抗原均具有良好的免疫原性，可作为诊断华支睾吸虫病的候选抗原。

关键词: 华支睾吸虫病, 排泄/分泌产物, 免疫原性, 血清学诊断

Abstract:

To compare the immunogenicity of excretory/secretory products of Clonorchis sinensis (CsESP) at different intervals and evaluate their diagnostic value for clonorchiasis. Adult C. sinensis were cultured in vitro, and the culture supernatants collected 0-24 hours and 24-48 hours were mixed to prepare CsESP-1 and CsESP-2 antigens, respectively. Mice were randomly divided into 4 groups: CsESP-1, CsESP-2, adjuvant and PBS groups. Mice in each group were subcutaneously immunized with the corresponding antigen. Blood samples were collected at weeks 0, 2, 4 and 6 post-immunization to prepare immune sera. ELISA was used to measure the antibody titers against CsESP and levels of IgG and IgG1. Additionally, ELISA was employed to detect the levels of CsESP-specific IgG and its subclasses in blood samples from healthy individuals and those infected with C. sinensis. SPSS 27.0 software was used to calculate sensitivity, specificity and Youden’s index. The receiver operating characteristic (ROC) curves and area under the ROC curve (AUC) were computed to evaluate the diagnostic efficacy of the antigens. Blood samples from healthy individuals (Cs^-) and those infected with C. sinensis (Cs⁺), Strongyloides stercoralis, Fasciola gigantica and malaria patients were tested for cross-reactivity using ELISA. Comparisons between two groups were conducted using the t-test, while paired ROC analysis was used for AUC comparisons. ELISA results showed that at week 6 post-immunization, the antibody titers against CsESP in the sera of mice in the CsESP-1 and CsESP-2 groups were 1:102 400 and 1:400, respectively, indicating superior immunogenicity of CsESP-1. At week 6 post-immunization, the A₄₅₀ values for specific IgG and IgG1 in the sera of mice in the CsESP-1 group were 0.926 and 1.803, respectively, both significantly higher than those in the adjuvant group (0.147 and 0.080, respectively) (t = 5.805, 5.643; both P < 0.05). In the CsESP-2 group, the A₄₅₀ values for specific IgG at weeks 2, 4 and 6 post-immunization were 0.279, 0.437 and 0.523, respectively, all higher than those in the adjuvant group (0.133, 0.127, 0.142) (t = 2.906, 5.286, 6.83; P < 0.05, 0.05, 0.01). The A₄₅₀ values for IgG1 in the CsESP-2 group at weeks 4 and 6 post-immunization were 0.225 and 0.332, respectively, both higher than those in the adjuvant group (0.095, 0.083) (t = 3.423, 2.485; both P < 0.05). In Cs⁺ blood samples, the A₄₅₀ values for CsESP-1-specific IgG, IgG2 and IgG4 were 0.817, 0.274 and 0.524, respectively, all higher than those in Cs^- blood samples (0.456, 0.102 and 0.103, respectively) (t = 7.184, 2.720, 5.634; all P < 0.01). For CsESP-2, the A₄₅₀ values in Cs⁺ blood samples for specific IgG, IgG1, IgG2 and IgG4 were 0.783, 0.132, 0.233 and 0.465, respectively, all higher than those in Cs^- blood samples (0.460, 0.068, 0.074 and 0.082, respectively) (t = 4.768, 2.519, 2.634, 4.991; P < 0.01, 0.05, 0.05, 0.01). The CsESP-1 antigen demonstrated the best overall performance in detecting IgG4 in Cs⁺ blood samples, with sensitivity, specificity and accuracy of 89.2%, 86.5% and 87.9%, respectively. Similarly, the CsESP-2 antigen showed the same sensitivity specificity and accuracy (89.2%, 86.5% and 87.9%, respectively) for detecting IgG4 in Cs⁺ samples. ROC curve analysis revealed that the CsESP-1 antigen had moderate diagnostic value for detecting IgG1 and IgG2 (both AUC > 0.7) and high diagnostic value for detecting IgG and IgG4 (both AUC > 0.9). The CsESP-2 antigen exhibited moderate diagnostic value for detecting IgG, IgG1 and IgG2 (all AUC > 0.7) and high diagnostic value for detecting IgG4 (AUC > 0.9). Paired ROC analysis indicated that the diagnostic efficacy of the CsESP-1 antigen for IgG and IgG1 was superior to that of the CsESP-2 antigen (z = 3.515, 2.149; P < 0.01, 0.05). Neither the CsESP-1 nor CsESP-2 antigens showed cross-reactivity with IgG in blood samples from individuals infected with S. stercoralis, F. gigantica or malaria patients. In conclusion, both the CsESP-1 and CsESP-2 antigens prepared in this study exhibited good immunogenicity and could serve as candidate antigens for the diagnosis of clonorchiasis.

Key words: Clonorchiasis, Excretory/secretory products, Immunogenicity, Serological diagnosis

中图分类号:

R532.23

吴雨洪, 邓雪玲, 黄世圣, 吴美欣, 罗柳春, 傅晓茵, 战廷正, 李青, 唐泽丽. 不同时段华支睾吸虫排泄分泌产物的免疫原性及其诊断价值[J]. 中国寄生虫学与寄生虫病杂志, 2025, 43(3): 440-445.

WU Yuhong, DENG Xueling, HUANG Shisheng, WU Meixin, LUO Liuchun, FU Xiaoyin, ZHAN Tingzheng, LI Qing, TANG Zeli. Immunogenicity of excretory/secretory products of Clonorchis sinensis at different stages and its diagnostic value for clonorchiasis[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2025, 43(3): 440-445.

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抗原	抗体类型	最大约登指数	临界值	敏感度/%	特异度/%	准确度/%
CsESP-1	IgG	0.703	0.569	89.2	81.1	85.1
	IgG1	0.730	0.063	81.1	91.9	86.5
	IgG2	0.351	0.083	86.5	48.6	67.6
	IgG4	0.757	0.135	89.2	86.5	87.9
CsESP-2	IgG	0.487	0.580	67.6	81.1	74.4
	IgG1	0.487	0.070	70.3	78.4	74.4
	IgG2	0.405	0.090	48.6	91.9	70.3
	IgG4	0.757	0.110	89.2	86.5	87.9

不同时段华支睾吸虫排泄分泌产物的免疫原性及其诊断价值

Immunogenicity of excretory/secretory products of Clonorchis sinensis at different stages and its diagnostic value for clonorchiasis

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