云南省洱源县人群芽囊原虫和卡耶塔环孢子虫感染情况及其分子特征

doi:10.12140/j.issn.1000-7423.2024.02.016

中国寄生虫学与寄生虫病杂志 ›› 2024, Vol. 42 ›› Issue (2): 242-250.doi: 10.12140/j.issn.1000-7423.2024.02.016

云南省洱源县人群芽囊原虫和卡耶塔环孢子虫感染情况及其分子特征

王雅雪¹(), 简金花¹^,², 刘华¹, 秦源¹, 彭晓雪¹, 苏雅馨¹, 沈玉娟¹^,³^,^*()

1 中国疾病预防控制中心寄生虫病预防控制所（国家热带病研究中心），传染病溯源预警与智能决策全国重点实验室，国家卫健委寄生虫病原与媒介生物学重点实验室，世界卫生组织热带病合作中心，国家级热带病国际联合中心，上海 200025
2 杭州医学院，浙江杭州 310000
3 上海交通大学医学院-国家热带病研究中心全球健康学院，上海 200025

收稿日期:2024-02-20 修回日期:2024-03-09 出版日期:2024-04-30 发布日期:2024-04-11
通讯作者: * 沈玉娟（1969—），女，硕士，研究员，从事肠道原虫分子流行病学、溯源和检测技术等研究。E-mail：shenyj@nipd.chinacdc.cn
作者简介:王雅雪（1999—），女，硕士研究生，从事肠道原虫分子流行病学研究。E-mail：yaxue_361@163.com
基金资助:
国家自然科学基金(82372283);国家自然科学基金(82072307);上海市加强公共卫生体系建设三年行动计划（2023—2025）重点学科项目(GWVI-11.1-09)

Infection of Blastocystis and Cyclospora cayetanensis in residents in Eryuan County, Yunnan Province and their molecular characterization

WANG Yaxue¹(), JIAN Jinhua¹^,², LIU Hua¹, QIN Yuan¹, PENG Xiaoxue¹, SU Yaxin¹, SHEN Yujuan¹^,³^,^*()

1 National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention; Chinese Center for Tropical Diseases Research; National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases; NHC Key Laboratory of Parasite and Vector Biology; WHO Collaborating Centre for Tropical Diseases; National Center for International Research on Tropical Diseases, Shanghai 200025, China
2 Hangzhou Medical College, Hangzhou 310000, Zhejiang, China
3 School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China

Received:2024-02-20 Revised:2024-03-09 Online:2024-04-30 Published:2024-04-11
Contact: * E-mail: shenyj@nipd.chinacdc.cn
Supported by:
National Natural Science Foundation of China(82372283);National Natural Science Foundation of China(82072307);Three-Year Initiative Plan for Strengthening Public Health System Construction in Shanghai (2023-2025) Key Discipline Project(GWVI-11.1-09)

摘要/Abstract

摘要：

目的了解云南省洱源县人群芽囊原虫和卡耶塔环孢子虫的感染情况及其分子特征，为寄生虫病防治工作提供参考。方法 2022年7—8月在云南省洱源县5个村庄采用简单随机抽样法抽取1岁以上的常住居民作为调查对象，采集调查对象新鲜粪样，收集其社会人口学信息。提取粪样DNA，使用普通PCR和巢式PCR分别扩增芽囊原虫和卡耶塔环孢子虫的核糖体小亚基RNA（SSU rRNA）基因，分析人群感染情况。对阳性PCR扩增产物进行双向测序，在NCBI进行BLAST比对分析，鉴定虫种和基因亚型，采用MEGA 11.0软件以邻接法构建系统进化树。用SPSS 21.0软件进行统计学分析，感染率的比较采用χ²检验或Fisher确切概率法。结果共采集100份居民粪样。芽囊原虫感染率为14.0%（14/100）。其中，男性、女性芽囊原虫感染率分别为14.6%（6/41）和13.6%（8/59）；60岁以上的居民和家庭人口数为6人及以上的感染率最高，分别为18.5%（5/27）、3/15；未接受过教育和小学文化者感染率较高，分别为2/11和17.0%（8/47）；感染者均为农民。不同性别、年龄、家庭人口数、教育水平和职业等人群的芽囊原虫感染率差异均无统计学意义（χ² = 0.023、2.730、2.235、1.404、1.668，均P > 0.05）。卡耶塔环孢子虫感染率为2.0%（2/100），感染者均为女性农民。未查见芽囊原虫和卡耶塔环孢子虫的混合感染。14份芽囊原虫阳性样本中扩增出ST1和ST3亚型序列各7条，其中7条ST1序列有25个核苷酸差异，5条与芽囊原虫（GenBank：ON932511、KU147348、MK801408、MW728079、OR754904）的序列一致性分别为100%，2条为新序列（GenBank：PP439288、PP439289），与芽囊原虫（GenBank：OP725964、KU147333）一致性为99.8%；7条ST3序列有1个核苷酸差异，与芽囊原虫（GenBank：KU147372、MK801366）的序列一致性分别为100%。扩增获得的2条卡耶塔环孢子虫序列相同，与卡耶塔环孢子虫（GenBank：KY770755）的序列一致性为100%。系统进化树显示，本研究中芽囊原虫分别与ST1和ST3亚型聚在一大分支上，卡耶塔环孢子与人源卡耶塔环孢子虫聚在同一分支上。结论云南省洱源县人群存在芽囊原虫和卡耶塔环孢子虫感染。芽囊原虫感染率较高，感染亚型为ST1和ST3亚型，ST1的遗传变异程度较高。

关键词: 芽囊原虫, 卡耶塔环孢子虫, 感染, 分子特征, 洱源县

Abstract:

Objective To investigate the prevalence and molecular characterizations of Blastocystis and Cyclospora cayetanensis in residents in Eryuan County, Yunnan Province to provide reference for parasitic disease control and prevention. Methods From July to August 2022, permanent residents over the age of 1 were enrolled for the survey by simple random sampling from the five villages in Eryuan County, Yunnan Province. Fresh fecal samples and their social demographic information were collected. The fecal genomic DNA was extracted, and the ribosomal small subunit RNA (SSU rRNA) genes of Blastocystis and C. cayetanensis were amplified by PCR and nested PCR, respectively, in order to analyze the prevalence in the residents. The positive products were sequenced bidirectionally, the species and gene subtypes were identified by BLAST alignment in NCBI. The phylogenetic trees were constructed using the neighbor-Joining method by MEGA 11.0 software. SPSS 21.0 software was used for statistical analysis, and the infection rates were compared by χ² test or Fisher’s exact probability method. Results A total of 100 fecal samples were obtained from residents, of which the Blastocystis infection rate was 14.0% (14/100). Among them, the Blastocystis infection rates in male and female were 14.6% (6/41) and 13.6% (8/59), respectively. Residents over 60 years old and the family size of 6 persons and above had the highest infection rate, which was 18.5% (5/27) and 3/15, respectively. The infection rates were 2/11 and 17.0% (8/47) for those with no education and only elementary school education, respectively. All the infected residents were farmers. There was no statistically significant difference in Blastocystis infection rate by gender, age, family size, education level and occupation (χ² = 0.023, 2.730, 2.235, 1.404, 1.668; all P > 0.05). The C. cayetanensis infection rate was 2.0% (2/100). All of the infected residents were female farmers. No mixed infection of Blastocystis and C. cayetanensis was detected. Both 7 ST1 and ST3 sequences were amplified from 14 Blastocystis-positive samples, of which 7 ST1 sequences had 25 nucleotide differences. Five sequences were 100% homology to the Blastocystis sequences (GenBank: ON932511, KU147348, MK801408, MW728079, OR754904); 2 were new sequences (GenBank: PP439288-PP439289), with 99.8% homology to the Blastocystis sequences (GenBank: OP725964, KU147333). There was 1 nucleotide difference within 7 ST3 sequences, with 100% homology to the Blastocystis sequences (GenBank: KU147372, MK801366). The 2 sequences of C. cayetanensis obtained were identical and showed 100% homology to the C. cayetanensis sequence (GenBank: KY770755). The phylogenetic trees showed that Blastocystis in this study clustered in large branches with gene subtype ST1 and ST3, respectively, and C. cayetanensis clustered in the same branch with C. cayetanensis of human origin. Conclusion Blastocystis and C. cayetanensis were detected in the residents of Eryuan County, Yunnan Province. The infection rate of Blastocystis was high, with the subtypes of ST1 and ST3, and the ST1 of Blastocystis reveals higher genetic variation.

Key words: Blastocystis, Cyclospora cayetanensis, Infection, Molecular characterization, Eryuan County

中图分类号:

R531.9

王雅雪, 简金花, 刘华, 秦源, 彭晓雪, 苏雅馨, 沈玉娟. 云南省洱源县人群芽囊原虫和卡耶塔环孢子虫感染情况及其分子特征[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(2): 242-250.

WANG Yaxue, JIAN Jinhua, LIU Hua, QIN Yuan, PENG Xiaoxue, SU Yaxin, SHEN Yujuan. Infection of Blastocystis and Cyclospora cayetanensis in residents in Eryuan County, Yunnan Province and their molecular characterization[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2024, 42(2): 242-250.

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	(梁霞霞, 邹扬, 李涛善, 等. 云岭牛毕氏肠微孢子虫和芽囊原虫分子流行病学调查研究[J]. 中国动物传染病学报, 2021, 29(5): 75-82.)
[46]	Han N, Peng XH, Qiang YJ, et al. Genetic characteristics of Blastocystis sp. ST3 at the genome level in the Chinese population[J]. Parasitol Res, 2023, 122(11): 2719-2727. doi: 10.1007/s00436-023-07973-6 pmid: 37715083
[47]	Cinar HN, Gopinath G, Murphy HR, et al. Molecular typing of Cyclospora cayetanensis in produce and clinical samples using targeted enrichment of complete mitochondrial genomes and next-generation sequencing[J]. Parasit Vectors, 2020, 13(1): 122.

人口学特征 Demographic characteristic	检查人数 No. examined	阳性例数（感染率/%) No. positive (Infection rate/%)	亚型（数量） Subtype (n)	χ² 值 χ² value	P值 P value
性别 Gender				0.023	0.879
男性 Male	41	6 (14.6)	ST1 (3), ST3 (3)
女性 Female	59	8 (13.6)	ST1 (4), ST3 (4)
年龄/岁 Age/Year				2.730	0.384^a
< 5	0	0
5~17	13	0 (0)
18~35	4	0 (0)
36~60	56	9 (16.1)	ST1 (5), ST3 (4)
> 60	27	5 (18.5)	ST1 (2), ST3 (3)
家庭人口数 Family size				2.235	0.568^a
3人及以下 Three persons and below	22	2 (9.1)	ST1 (1), ST3 (1)
4人 Four persons	31	6 (19.4)	ST1 (3), ST3 (3)
5人 Five persons	32	3 (9.4)	ST1 (1), ST3 (2)
6人及以上 Six persons and above	15	3/15	ST1 (2), ST3 (1)
民族 Ethnic group				0.434	0.596
白族 Bai	92	14 (15.2)	ST1 (7), ST3 (7)
汉族 Han	8	0 (0)
职业 Occupation				1.668	0.197
农民 Farmer	85	14 (16.5)	ST1 (7), ST3 (7)
非农民^b Non-farmer^b	15	0 (0)
教育水平 Educational level				1.404	0.788^a
未接受教育 Uneducated	11	2/11	ST1 (1), ST3 (1)
小学 Elementary school	47	8 (17.0)	ST1 (3), ST3 (5)
初中 Junior high school	33	3 (9.1)	ST1 (2), ST3 (1)
高中及以上 Senior high school and above	9	1/9	ST1 (1)
总计 Total	100	14 (14.0)	ST1 (7), ST3 (7)

分离株编号 Isolate number	GenBank号 GenBank ID	核苷酸位点Nucleotide positions
分离株编号 Isolate number	GenBank号 GenBank ID	36	37	186	188	194	197	198	199	200	209	210	211	214	215	216	217	219	220	221	222	223	224	243	268	281
EY96	PP439288^a	C	A	A	C	-	T	G	A	G	C	T	C	G	A	C	A	T	A	A	G	T	C	A	T	A
EY21	OP725948	A	C	A	C	-	T	G	A	G	C	T	C	G	A	C	A	T	A	A	G	T	C	G	C	C
EY30	PP439289	A	C	G	-	C	A	G	T	A	T	A	G	A	G	A	T	A	T	C	A	C	T	G	T	C
EY75	KU147348	C	A	A	C	-	T	G	A	G	C	T	C	G	A	C	A	T	A	A	G	T	C	G	T	G
EY77	MK801408	C	A	G	-	C	A	A	T	G	T	A	G	A	G	A	T	A	T	C	A	C	T	G	T	C
EY78	MW728079	C	A	A	C	-	T	G	A	G	C	T	C	G	A	C	A	T	A	A	G	T	C	G	T	C
EY81	OR754904	A	C	A	C	-	T	G	A	G	C	T	C	G	A	C	A	T	A	A	G	T	C	G	C	C

年份 Year	地区 Region	人群 Population	检测方法 Detection method	检查数No. examined	阳性数No. positive	感染率/% Infection rate/%	亚型（数量） Subtype (n)	参考文献 Reference
1994	云南省 Yunnan Province	常住居民 Permanent residents	碘液涂片 Iodine smear	53 061	2 390	4.5	-	[15]
2007	大理 Dali	普通村民 Ordinary villagers	体外培养 + PCR In vitro cul-ture + PCR	407	75	18.4	ST3 (38), ST1 (22), ST2(6), ST1/3 (5), ST2/3 (1), 未知 Unknown (3)	[16]
2007	西双版纳 Xishuangbanna	普通村民 Ordinary villagers	体外培养 + PCR In vitro cul-ture + PCR	239	78	32.6	ST3 (55), ST1 (16), ST2 (1), ST4 (1), ST1/2 (1), ST1/3 (1), 未知 Unknown (3)	[17]
2008	西双版纳 Xishuangbanna	普通村民 Ordinary villagers	涂片 Smear	215	43	20.0	-	[18]
2016	昆明 Kunming	腹泻儿童 Diarrheal children	PCR	850	26	3.1	-	[19]
2016	昆明 Kunming	健康儿童 Healthy children	PCR	170	1	0.6	-	[19]
2016	昆明 Kunming	腹泻患者 Diarrheal patients	PCR	1 121	47	4.2	ST1 (46), ST2 (1)	[20]
2016	昆明 Kunming	非腹泻患者 Non-diarrheal patients	PCR	319	11	3.5	ST1 (11)	[20]
2018	腾冲 Tengchong	HIV携带者 HIV carriers	PCR	324	12	3.7	ST1 (3), ST4 (3), ST7 (3), ST3 (2), ST12 (1)	[21]
2019	西双版纳 Xishuangbanna	瑶族村民 Yao villagers	PCR	289	13	4.5	ST3 (8), ST1 (3), ST4 (1), 未知 Unknown (1)	[22]
2021	大理 Dali	在校大学生 College students	PCR	426	6	1.4	ST1 (6)	[23]
合计 Total				57 421	2 702	4.7	ST1 (107), ST3 (103), ST2 (8), ST4 (5), ST1/3 (6), ST1/2 (1), ST2/3 (1), 未知 Unknown (7)

云南省洱源县人群芽囊原虫和卡耶塔环孢子虫感染情况及其分子特征

Infection of Blastocystis and Cyclospora cayetanensis in residents in Eryuan County, Yunnan Province and their molecular characterization

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