我国局部地区隐孢子虫分子流行病学研究
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摘要
隐孢子虫病为重要的新发人兽共患传染病,已发现于106个国家的人体病例,是人体急性腹泻或慢性致死性腹泻的重要致病因素。隐孢子虫感染包括人在内的260多种动物,可通过粪-口途径、直接接触或食入污染的食物或饮水进行传播。隐孢子虫属具有广泛的遗传多态性,除了23个已被承认的有效种,尚存在至少74个未界定种名的基因型。目前,对隐孢子虫病尚无有效的治疗药物或疫苗,因而该病严重影响到动物的生长和发育以及人类的健康,造成巨大经济损失。1993年,美国密尔奥基市隐孢子虫病暴发导致40多万人被感染,100多人死亡,直接经济损失达9620万美元。研究隐孢子虫的流行以及种类/基因型/亚型分布对了解隐孢子虫的传播以及防控隐孢子虫病具有重要的意义。本研究从流行病学调查、种类/基因型鉴定、亚型分型、群体遗传结构分析4个层次对我国河南、四川、陕西、广西、黑龙江、吉林6个省份进行了隐孢子虫分子流行病学研究。
1.奶牛隐孢子虫流行病学调查,粪便中隐孢子虫卵囊的检测使用饱和蔗糖溶液漂浮法和改良抗酸染色法。
显微镜检测显示,河南省奶牛隐孢子虫平均感染率为13.0%(276/2116)。断奶前、3-11月龄、12-24月龄、大于24月龄奶牛隐孢子虫感染率分别为21.5%(172/801)、11.3%(86/758)、5.7%(15/262)、1.0%(3/295)(ρ<0.01)。断奶前犊牛隐孢子虫感染率在夏季最高(50%),冬季最低(17.3%)(ρ>0.05)。
2.隐孢子虫样品基因分型采用基于SSU rRNA基因的限制性片段长度多态性(RFLP)分析以及DNA序列分析,限制性内切酶包括SspI,VspI和MboII。
成功基因分型644个动物源(奶牛、猪、鸡、鸭、鸵鸟)和人源隐孢子虫阳性样品,鉴定出11个种类/基因型,包括C. parvum(n=54),C. bovi(sn=85),C. ryana(en=19),C. andersoni(n=96),C. suis(n=94),pig genotype II(n=14),C. baileyi(n=237),C. meleagridis(n=3),C. muris(n=10),C. hominis(n=9),C. felis(n=1)和犊牛隐孢子虫混合感染病例(n=22)。其中,奶牛源C. parvum和C. andersoni、禽源C. muris和C. meleagridis、猪源C. suis和pig genotype II为人兽共患种类/基因型,具有以动物-人传播途径的人兽共患传播风险。人体感染C. hominis和C. felis表明在研究地区存在人-人和动物-人两种传播途径。
在断奶前犊牛,C. bovis是最为常见的隐孢子虫种类,发现于所有周龄段的犊牛;其次为C. parvum,分布于7个周龄段;C. bovis和C. parvum在断奶前犊牛隐孢子虫阳性样品中所占的比例分别为37.8%和31.4%。相对地,在断奶后犊牛(3-11月龄)、青年牛(12-24月龄)和成年奶牛(大于24月龄),C. andersoni最为常见而C. bovis仅发现于3-11月龄犊牛。
C. suis为猪寄生的优势隐孢子虫种类;除了3-6月龄猪未发现隐孢子虫感染,其它各年龄群的猪均鉴定出2个种类/基因型(C. suis和pig genotype II);C. suis更常见于幼龄猪,而在大于6月龄猪中,pig genotype II比C. suis相对常见。C. baileyi为禽类隐孢子虫感染的优势种类,发现于所有年龄群的鸡以及11-50日龄雏鸭;相对地,C. meleagridis仅分布于31-120日龄蛋鸡;在鸵鸟,C. baileyi发现于1岁以下鸵鸟而C. muris发现于1岁以上鸵鸟。人体隐孢子虫优势感染种类为C. hominis,主要来源于6岁以下的婴幼儿。
断奶前犊牛隐孢子虫种类季节变化研究显示,除了春季,C. parvum和C. bovis分布在各季节之间存在显著性差异,C. parvum优势流行于夏季,而C. bovis常见于秋季和冬季(ρ<0.01)。
3. C. parvum和C. hominis亚型分型采用DNA序列分析60kDa糖蛋白(gp60)基因。在断奶前犊牛,测序分析gp60基因显示67个C. parvum样品均属同一亚型IIdA19G1。相对地,在9个C. hominis样品中鉴定出3个亚型家族Ia (n=1), Ib (n =6)和Id (n=2)。在亚型家族Ib中,发现3个亚型IbA16G2 (n=1),IbA19G2 (n=2)和IbA20G2 (n=3)。Ia和Id亚型家族分别只发现1个亚型,即IaA9R3 (n=1)和IdA21 (n=2)。
4. C. muris和C. andersoni群体遗传结构分析采用基于小卫星MS1,MS2,MS3和MS16基因的多位点序列分型技术(MLST)以及对获得的MLST数据使用生物信息学软件进行统计分析的方法。
对河南、四川、陕西、广西、黑龙江和吉林地区不同动物来源的52个C. muris和C. andersoni样品进行了多位点序列分型。9个C. muris和42个C. andersoni样品在所有4个位点均被成功分型,发现7个新亚型,形成了2个C. muris和10个C. andersoni MLST亚型。其中,MLST亚型(4-4-4-1)为牛源C. andersoni的优势亚型类型。不同动物(鼠、鸵鸟、牛、绵羊、骆驼)来源的C. muris和C. andersoni其MLST亚型具有差异性并呈现出地理区域性分布特征。群体遗传分析表明,我国牛源C. andersoni为流行性群体结构。
综上所述,本研究对河南省奶牛隐孢子虫进行了系统的流行病学调查;分析了河南省主要畜禽和人体隐孢子虫样品的种类/基因型/亚型分布;研究了我国局部地区C. muris和C. andersoni群体遗传结构。研究结果不仅具有学术价值,而且具有重要的公共卫生意义。另外,研究结果为进一步研究我国不同地区隐孢子虫分子流行病学以及有效防控我国隐孢子虫病提供了参考资料。
Cryptosporidiosis is an recently emerging zoonotic infectious disease, which has been found in human cases in 106 countries and it is an important factor for acute diarrhea or chronic lethal diarrhea. Cryptosporidium spp. can infect more than 260 animals, including humans. It can be transmitted by the fecal-oral route, via either direct contact or ingestion of contaminated food or water. There is extensive genetic variation within the genus Cryptosporidium, in addition to 23 recognized species of Cryptosporidium, 74 Cryptosporidium genotypes with no designated species names have been described. Currently, no effective drug or vaccine is available for cryptosporidiosis. Thus, this disease seriously affects the growth and development of animals and human health, causing huge economic losses. In 1993, the outbreak of cryptosporidiosis occurred in Miwakkeii city in the United States has led to infections of 400,000 persons and more than 100 individuals were died, with the direct economic losses amounting to $ 96,200,000. Researches on the prevalence of Cryptosporidium spp. and the distribution of Cryptosporidium species/genotype/subtypes have important implications in understanding the spread of Cryptosporidium and the prevention and control of cryptosporidiosis. In the present study, molecular epidemiology study of Cryptosporidium was performed in six provinces (Henan, Sichuan, Shanxi, Guangxi, Heilongjiang, and Jilin) at four levels, i.e., epidemiological survey, species/genotype identification, subtype typing, and population genetic structure analysis.
1. Sheather’s sugar flotation technique and modified acid-fast stain method were used to detect the Cryptosporidium oocysts in faeces of dairy cattle in epidemiological survey.
Microscopic examination showed that the overall infection rate of Cryptosporidium spp. was 13.0% (276/2116) in dairy cattle in Henan province. The infection rate of Cryptosporidium spp. was 21.5% (172/801), 11.3% (86/758), 5.7% (15/262), and 1.0% (3/295) in pre-weaned, 3-11-month-old, 12-24-month-old, and more than 24-month-old dairy cattle, respectively (ρ< 0.01). The highest infection rate (50%) of Cryptosporidium spp. in pre-weaned calves was seen in summer and the lowest (17.3%) in winter (ρ> 0.05).
2. Cryptosporidium samples were genotyped by restriction fragment length polymorphism (RFLP) analysis and DNA sequence analysis of the SSU rRNA gene, with the restriction enzyme SspI, VspI, and MboII being included.
A total of 644 Cryptosporidium-positive samples from animals (dairy cattle, pigs, chichens, ducks, and ostriches) and humans were successfully genotyped and eleven Cryptosporidium species/genotypes were identified, including C. parvum (n=54), C. bovis (n=85), C. ryanae (n=19), C. andersoni (n=96), C. suis (n=94), pig genotype II (n= 14), C. baileyi (n=237), C. meleagridis (n=3), C. muris (n=10), C. hominis (n=9), C. felis (n=1), and Cryptosporidium mixed infections in calves (n=22). Among which, the C. parvum and C. andersoni in dairy cattle, the C. muris and C. meleagridis in birds, the C. suis and pig genotype II in pigs are zoonotic species/genotypes, having the risks of zoonotic transmission by animal-human route. That C. hominis and C. felis were detected in humans indicated that there existed two types of transmission route by human-human and animal-human in the areas studied.
In pre-weaned calves, Cryptosporidium bovis was the most commonly identified Cryptosporidium and was found in all weekly age groups; C. parvum was the second most common species and was detected in seven age groups; the ratio of C. bovis and C. parvum were respectively 37.8% and 31.4% among all the Cryptosporidium-positive samples detected in pre-weaned calves. In contrast, C. andersoni was the most common Cryptosporidium species in post-weaned calves (3-11-month-old), heifers (12-24-month-old), and adult dairy cattle (more than 24 months of age), whereas C. bovis was only seen in 3 to 11-month-old calves. Cryptosporidium suis was the predominant Cryptosporidium species in pigs; except for 3 to 6-month-old pigs, the remaining age groups were all positive for two Cryptosporidium species/genotypes (C. suis and Cryptosporidium pig genotype II); C. suis was more often seen in younger pigs whereas the Cryptosporidium pig genotype II was relatively often seen in more than 6-month-old pigs. C. baileyi was the predominant species of Cryptosporidium detected in birds and was found in all age groups of chickens and 11 to 50-day-old ducks; in contrast, C. meleagridis were only identified in 31 to 120-day-old layer chickens. In ostriches, C. baileyi was found in lower than 1-year-old ostriches whereas C. muris was detected in more than 1-year-old ostriches. C. hominis was the predominant Cryptosporidium species in humans, mainly coming from infants/children under six years of age.
Seasonal variation of Cryptosporidium species in pre-weaned calves showed that except for spring, the distribution of Cryptosporidium spp. differed significantly among seasons, with C. parvum dominating in summer and C. bovis in autumn and winter (ρ< 0.01).
3. Subtyping of C. parvum and C. hominis was done by DNA sequence analysis of the 60 kDa glucoprotein (gp60) gene.
In pre-weaned calves, sequencing analysis of the gp60 gene showed that 67 C. parvum samples all belonged to subtype IIdA19G1. In contrast, three subtype families were identified in the nine C. hominis samples: Ia (n=1), Ib (n=6), and Id (n=2). Among subtype family Ib, three subtypes were found: IbA16G2 (n=1), IbA19G2 (n=2), and IbA20G2 (n=3). Only one subtype each was present in subtype families Ia and Id: IaA9R3 (n=1) and IdA21 (n=2).
4. Population genetic structure analysis of C. muris and C. andersoni was done by multilocus sequence typing (MLST) technique based on minisatellite sequences of MS1, MS2, MS3, and MS16 genes, and statistical analysis of the MLST data obtained by bioinformatics software.
Fifty two C. muris and C. andersoni samples from different animals in Henan, Sichuan, Shanxi, Guangxi, Heilongjiang, and Jilin were typed by MLST technique. In total, nine C. muris isolates and 42 C. andersoni samples were successfully typed at all four genetic loci. Seven new subtypes were found and consisted of two C. muris and 10 C. andersoni MLST subtypes. Among which, the MLST subtype (4-4-4-1) was the predominant subtype of C. andersoni in cattle. The MLST subtypes of C. muris and C. andersoni differed in different animals (mice, ostriches, cattle, sheep, and camel), and there existed geographic distribution characterization. Population genetic analysis showed that cattle-derived C. andersoni in China was epidemic population structure.
In summary, in this study, systematic epidemiological investigation of Cryptosporidium was performed in dairy cattle in Henan province; analyzing the distribution of Cryptosporidium species/genotype/subtypes in major livestock, poultry, and humans in Henan province; studying the population genetic structure of C. muris and C. andersoni in partial areas of China. Thus, the results have both academic value and important public health significance. In addition, the results also provided useful references for further studying the molecular epidemiology of Cryptosporidium in different areas, and for the effective prevention and control of cryptosporidiosis in China.
1.奶牛隐孢子虫流行病学调查,粪便中隐孢子虫卵囊的检测使用饱和蔗糖溶液漂浮法和改良抗酸染色法。
显微镜检测显示,河南省奶牛隐孢子虫平均感染率为13.0%(276/2116)。断奶前、3-11月龄、12-24月龄、大于24月龄奶牛隐孢子虫感染率分别为21.5%(172/801)、11.3%(86/758)、5.7%(15/262)、1.0%(3/295)(ρ<0.01)。断奶前犊牛隐孢子虫感染率在夏季最高(50%),冬季最低(17.3%)(ρ>0.05)。
2.隐孢子虫样品基因分型采用基于SSU rRNA基因的限制性片段长度多态性(RFLP)分析以及DNA序列分析,限制性内切酶包括SspI,VspI和MboII。
成功基因分型644个动物源(奶牛、猪、鸡、鸭、鸵鸟)和人源隐孢子虫阳性样品,鉴定出11个种类/基因型,包括C. parvum(n=54),C. bovi(sn=85),C. ryana(en=19),C. andersoni(n=96),C. suis(n=94),pig genotype II(n=14),C. baileyi(n=237),C. meleagridis(n=3),C. muris(n=10),C. hominis(n=9),C. felis(n=1)和犊牛隐孢子虫混合感染病例(n=22)。其中,奶牛源C. parvum和C. andersoni、禽源C. muris和C. meleagridis、猪源C. suis和pig genotype II为人兽共患种类/基因型,具有以动物-人传播途径的人兽共患传播风险。人体感染C. hominis和C. felis表明在研究地区存在人-人和动物-人两种传播途径。
在断奶前犊牛,C. bovis是最为常见的隐孢子虫种类,发现于所有周龄段的犊牛;其次为C. parvum,分布于7个周龄段;C. bovis和C. parvum在断奶前犊牛隐孢子虫阳性样品中所占的比例分别为37.8%和31.4%。相对地,在断奶后犊牛(3-11月龄)、青年牛(12-24月龄)和成年奶牛(大于24月龄),C. andersoni最为常见而C. bovis仅发现于3-11月龄犊牛。
C. suis为猪寄生的优势隐孢子虫种类;除了3-6月龄猪未发现隐孢子虫感染,其它各年龄群的猪均鉴定出2个种类/基因型(C. suis和pig genotype II);C. suis更常见于幼龄猪,而在大于6月龄猪中,pig genotype II比C. suis相对常见。C. baileyi为禽类隐孢子虫感染的优势种类,发现于所有年龄群的鸡以及11-50日龄雏鸭;相对地,C. meleagridis仅分布于31-120日龄蛋鸡;在鸵鸟,C. baileyi发现于1岁以下鸵鸟而C. muris发现于1岁以上鸵鸟。人体隐孢子虫优势感染种类为C. hominis,主要来源于6岁以下的婴幼儿。
断奶前犊牛隐孢子虫种类季节变化研究显示,除了春季,C. parvum和C. bovis分布在各季节之间存在显著性差异,C. parvum优势流行于夏季,而C. bovis常见于秋季和冬季(ρ<0.01)。
3. C. parvum和C. hominis亚型分型采用DNA序列分析60kDa糖蛋白(gp60)基因。在断奶前犊牛,测序分析gp60基因显示67个C. parvum样品均属同一亚型IIdA19G1。相对地,在9个C. hominis样品中鉴定出3个亚型家族Ia (n=1), Ib (n =6)和Id (n=2)。在亚型家族Ib中,发现3个亚型IbA16G2 (n=1),IbA19G2 (n=2)和IbA20G2 (n=3)。Ia和Id亚型家族分别只发现1个亚型,即IaA9R3 (n=1)和IdA21 (n=2)。
4. C. muris和C. andersoni群体遗传结构分析采用基于小卫星MS1,MS2,MS3和MS16基因的多位点序列分型技术(MLST)以及对获得的MLST数据使用生物信息学软件进行统计分析的方法。
对河南、四川、陕西、广西、黑龙江和吉林地区不同动物来源的52个C. muris和C. andersoni样品进行了多位点序列分型。9个C. muris和42个C. andersoni样品在所有4个位点均被成功分型,发现7个新亚型,形成了2个C. muris和10个C. andersoni MLST亚型。其中,MLST亚型(4-4-4-1)为牛源C. andersoni的优势亚型类型。不同动物(鼠、鸵鸟、牛、绵羊、骆驼)来源的C. muris和C. andersoni其MLST亚型具有差异性并呈现出地理区域性分布特征。群体遗传分析表明,我国牛源C. andersoni为流行性群体结构。
综上所述,本研究对河南省奶牛隐孢子虫进行了系统的流行病学调查;分析了河南省主要畜禽和人体隐孢子虫样品的种类/基因型/亚型分布;研究了我国局部地区C. muris和C. andersoni群体遗传结构。研究结果不仅具有学术价值,而且具有重要的公共卫生意义。另外,研究结果为进一步研究我国不同地区隐孢子虫分子流行病学以及有效防控我国隐孢子虫病提供了参考资料。
Cryptosporidiosis is an recently emerging zoonotic infectious disease, which has been found in human cases in 106 countries and it is an important factor for acute diarrhea or chronic lethal diarrhea. Cryptosporidium spp. can infect more than 260 animals, including humans. It can be transmitted by the fecal-oral route, via either direct contact or ingestion of contaminated food or water. There is extensive genetic variation within the genus Cryptosporidium, in addition to 23 recognized species of Cryptosporidium, 74 Cryptosporidium genotypes with no designated species names have been described. Currently, no effective drug or vaccine is available for cryptosporidiosis. Thus, this disease seriously affects the growth and development of animals and human health, causing huge economic losses. In 1993, the outbreak of cryptosporidiosis occurred in Miwakkeii city in the United States has led to infections of 400,000 persons and more than 100 individuals were died, with the direct economic losses amounting to $ 96,200,000. Researches on the prevalence of Cryptosporidium spp. and the distribution of Cryptosporidium species/genotype/subtypes have important implications in understanding the spread of Cryptosporidium and the prevention and control of cryptosporidiosis. In the present study, molecular epidemiology study of Cryptosporidium was performed in six provinces (Henan, Sichuan, Shanxi, Guangxi, Heilongjiang, and Jilin) at four levels, i.e., epidemiological survey, species/genotype identification, subtype typing, and population genetic structure analysis.
1. Sheather’s sugar flotation technique and modified acid-fast stain method were used to detect the Cryptosporidium oocysts in faeces of dairy cattle in epidemiological survey.
Microscopic examination showed that the overall infection rate of Cryptosporidium spp. was 13.0% (276/2116) in dairy cattle in Henan province. The infection rate of Cryptosporidium spp. was 21.5% (172/801), 11.3% (86/758), 5.7% (15/262), and 1.0% (3/295) in pre-weaned, 3-11-month-old, 12-24-month-old, and more than 24-month-old dairy cattle, respectively (ρ< 0.01). The highest infection rate (50%) of Cryptosporidium spp. in pre-weaned calves was seen in summer and the lowest (17.3%) in winter (ρ> 0.05).
2. Cryptosporidium samples were genotyped by restriction fragment length polymorphism (RFLP) analysis and DNA sequence analysis of the SSU rRNA gene, with the restriction enzyme SspI, VspI, and MboII being included.
A total of 644 Cryptosporidium-positive samples from animals (dairy cattle, pigs, chichens, ducks, and ostriches) and humans were successfully genotyped and eleven Cryptosporidium species/genotypes were identified, including C. parvum (n=54), C. bovis (n=85), C. ryanae (n=19), C. andersoni (n=96), C. suis (n=94), pig genotype II (n= 14), C. baileyi (n=237), C. meleagridis (n=3), C. muris (n=10), C. hominis (n=9), C. felis (n=1), and Cryptosporidium mixed infections in calves (n=22). Among which, the C. parvum and C. andersoni in dairy cattle, the C. muris and C. meleagridis in birds, the C. suis and pig genotype II in pigs are zoonotic species/genotypes, having the risks of zoonotic transmission by animal-human route. That C. hominis and C. felis were detected in humans indicated that there existed two types of transmission route by human-human and animal-human in the areas studied.
In pre-weaned calves, Cryptosporidium bovis was the most commonly identified Cryptosporidium and was found in all weekly age groups; C. parvum was the second most common species and was detected in seven age groups; the ratio of C. bovis and C. parvum were respectively 37.8% and 31.4% among all the Cryptosporidium-positive samples detected in pre-weaned calves. In contrast, C. andersoni was the most common Cryptosporidium species in post-weaned calves (3-11-month-old), heifers (12-24-month-old), and adult dairy cattle (more than 24 months of age), whereas C. bovis was only seen in 3 to 11-month-old calves. Cryptosporidium suis was the predominant Cryptosporidium species in pigs; except for 3 to 6-month-old pigs, the remaining age groups were all positive for two Cryptosporidium species/genotypes (C. suis and Cryptosporidium pig genotype II); C. suis was more often seen in younger pigs whereas the Cryptosporidium pig genotype II was relatively often seen in more than 6-month-old pigs. C. baileyi was the predominant species of Cryptosporidium detected in birds and was found in all age groups of chickens and 11 to 50-day-old ducks; in contrast, C. meleagridis were only identified in 31 to 120-day-old layer chickens. In ostriches, C. baileyi was found in lower than 1-year-old ostriches whereas C. muris was detected in more than 1-year-old ostriches. C. hominis was the predominant Cryptosporidium species in humans, mainly coming from infants/children under six years of age.
Seasonal variation of Cryptosporidium species in pre-weaned calves showed that except for spring, the distribution of Cryptosporidium spp. differed significantly among seasons, with C. parvum dominating in summer and C. bovis in autumn and winter (ρ< 0.01).
3. Subtyping of C. parvum and C. hominis was done by DNA sequence analysis of the 60 kDa glucoprotein (gp60) gene.
In pre-weaned calves, sequencing analysis of the gp60 gene showed that 67 C. parvum samples all belonged to subtype IIdA19G1. In contrast, three subtype families were identified in the nine C. hominis samples: Ia (n=1), Ib (n=6), and Id (n=2). Among subtype family Ib, three subtypes were found: IbA16G2 (n=1), IbA19G2 (n=2), and IbA20G2 (n=3). Only one subtype each was present in subtype families Ia and Id: IaA9R3 (n=1) and IdA21 (n=2).
4. Population genetic structure analysis of C. muris and C. andersoni was done by multilocus sequence typing (MLST) technique based on minisatellite sequences of MS1, MS2, MS3, and MS16 genes, and statistical analysis of the MLST data obtained by bioinformatics software.
Fifty two C. muris and C. andersoni samples from different animals in Henan, Sichuan, Shanxi, Guangxi, Heilongjiang, and Jilin were typed by MLST technique. In total, nine C. muris isolates and 42 C. andersoni samples were successfully typed at all four genetic loci. Seven new subtypes were found and consisted of two C. muris and 10 C. andersoni MLST subtypes. Among which, the MLST subtype (4-4-4-1) was the predominant subtype of C. andersoni in cattle. The MLST subtypes of C. muris and C. andersoni differed in different animals (mice, ostriches, cattle, sheep, and camel), and there existed geographic distribution characterization. Population genetic analysis showed that cattle-derived C. andersoni in China was epidemic population structure.
In summary, in this study, systematic epidemiological investigation of Cryptosporidium was performed in dairy cattle in Henan province; analyzing the distribution of Cryptosporidium species/genotype/subtypes in major livestock, poultry, and humans in Henan province; studying the population genetic structure of C. muris and C. andersoni in partial areas of China. Thus, the results have both academic value and important public health significance. In addition, the results also provided useful references for further studying the molecular epidemiology of Cryptosporidium in different areas, and for the effective prevention and control of cryptosporidiosis in China.
引文
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