台灣地區低致病性禽流感H5亞型病毒及2009年流行之H1N1病毒在肉豬及禽畜業工作人員的血清偵測

蔡孟玲

doi:10.6342/NTU.2011.00484

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台湾地区低致病性禽流感H5亚型病毒及2009年流行之H1N1病毒在肉猪及禽畜业工作人员的血清侦测

Serological Surveillance on 2009 Pandemic Influenza H1N1 Viruses and LPAI H5 among Swine and Animal-related Workers in Taiwan

蔡孟玲 , 硕士　　导师：金传春　　

英文 DOI： 10.6342/NTU.2011.00484

流行性感冒；血清学侦测； 2009年新型流感；低致病性H5亚型禽流感；猪；动物相关产业人员；牧场；跨种传播；人畜共通传染病；全球流行；台湾； influenza virus ； serological surveillance ； pH1N1/09 ； LPAI H5 ； swine ； animal-related people ； farm ； inter-species transmission ； zoonosis ； pandemic ； Taiwan

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摘要 │ 参考文献 (121) │ 国际计量

摘要〈TOP〉

流行性感冒(简称流感)病毒具八段基因，且极易发生抗原漂变(drift)、移变(shift)及基因重组，因此常在动物或人群间变异传播、适应而造成大规模流行。台湾家禽曾出现「低」致病性禽流感H5亚型(简称LPAI H5)的流行，在2003年造成农业经济损失甚钜。而2009年美洲冒出禽、人、猪三重组的新型流感H1N1病毒(简称pH1N1/09)，即在猪群上经重组後，迅速适应而传播至人，终造成人际间全球大流行。由於猪呼吸道细胞可同时感染来自禽及人两宿主的流感病毒，致使猪可成为流感病毒基因重组与种间传播的媒介。本研究目的以血清学监测台湾肉猪及禽畜业相关人员对2009年新型H1N1病毒及本土低致病性H5禽流感病毒的感染，期能了解流感病毒可能跨越两宿主族群传播的关系与感染的危险/保护因子。
内容含三部分：(一) 2008到2010年间，在A县牧场内收集846支经济用猪血清，进行LPAI H5及pH1N1/09的血清抗体监测；（二）2010年收集同县1,354名禽畜业人员血清也进行此两流感病毒的抗体监测；及（三）找出人与猪感染之危险及保护因子。作法上，禽流感病毒的血球凝集抑制(hemagglutination inhibition, HI)抗体测试是采自2008年A县活禽市场分离得的LPAI H5病毒，并测血清对马红血球凝集抑制力(抗体效价≧1:20为阳性)；pH1N1/09的HI抗体是采自备制新流感疫苗的2009年A/California/7/2009 (H1N1)病毒株，以其对火鸡红血球凝集抑制力(抗体效价≧1:40为阳性)。
结果发现，自2008年8月到2010年5月间，猪只的此新流感H1N1病毒抗体总盛行率为19.1% (162/846) [三年各为8.9% (20/225)、2009年8月3.4% (10/291)及40.0% (132/330) ]；而猪场的此病毒抗体总盛行率为51.7% (31/60)[各为53.3% (8/15)、22.7% (5/22)及78.3% (18/23)]；均远高出该猪群/猪场的本土低致病性H5抗体总盛行率(p<0.0001)，且仅一只来自2008年的猪为低致病性H5抗体阳性(0.12%，1/846)。多变项分析控制年度变项後，发现此三年猪饲养於沿海区为其感染此新流感H1N1病毒的危险因子 [胜算比(Odds Ratio, OR)=2.33，95% 信赖区间(confidence interval, CI)=1.51-3.59，p=0.0001]，而良好的饲养管理为保护因子(OR=0.99，95% CI=0.98-0.995，p=0.0006)。以多变项分析单2010年检测结果後，发现另有非一贯式饲养也是危险因子(OR=2.88，95% CI=1.45-5.72，p=0.0025)，其余结果雷同(养於沿海：OR=3.43，95% CI=1.71-6.88，p=0.0005；管理好：OR=0.96 ，95% CI=0.95-0.97，p<0.0001)。
2010年10月动物相关产业人员的此新H1N1流感病毒抗体总盛行率为21.42% (290/1,354)，而未打新流感疫苗的之此病毒抗体阳性率为16.4% (138/841)，均高於其低致病性H5抗体阳性率1.77% (24/1,354) (p<0.0001)。以多变项分析控制年龄及打pH1N1/09疫苗两变项後，发现猪相关工作者的pH1N1/09抗体阳性风险较其他人员为高(OR=1.50，95% CI=1.11-2.02，p=0.0084)，而牧场场主(OR=0.071，95% CI=0.50-0.99，p=0.042)、屠夫或营业员(OR=0.32，95% CI=0.14-0.73，p=0.0061)为保护因子；在未打新流感疫苗者控制年龄後，牧场员工(OR=1.62，95% CI= 1.06- 2.47，p=0.0257)及兽医师(OR=4.72，95% CI=1.51-14.83，p=0.0078)较易感染；相反地，较高的身体质量指数(Body Mass Index，BMI) (OR=0.91，95% CI= 0.86- 0.97，p=0.003)及从事禽工作(OR=0.64，95% CI=0.43-0.96，p=0.0299)较不易感染。另控制年龄後，人感染低致病性H5流感的危险因子为从事禽业(OR= 3.40，95% CI=1.21-9.56，p=0.0205)，而保护因子为居住在猪舍密度较高(≧1.58 pig house/km2)区(OR=0.28，95% CI=0.11-0.76，p=0.0121)。
本研究的结论是2009年新流感病毒较禽流感H5病毒极易在台湾中部跨越感染人及猪群，因外来新流感H1N1大流行後期的台湾猪群抗体盛行率明显高於2009年第一波流行及2008年的背景值；反之，台湾禽的本土低致病性H5禽流感病毒较少在猪群间感染。有监於猪为流感病毒跨宿主传播与基因重组的重要桥梁，未来更应加强猪及相关产业人员的流感病毒及血清侦测，且将同牧场的猪群及人群配对比较，迅速掌握流感病毒在台湾禽畜业的动向；并探究新流感病毒是否较动物流感病毒有取代优势力及其机转。

并列摘要〈TOP〉

Influenza A viruses (IAVs) involving eight gene segments can infect many different hosts and are capable to have inter-species transmission among mammals, avian and humans. These viruses have changed continuously year by year and are also capable to emerge novel virus after antigenic shift occasionally. Pigs having receptors for both avian and mammalian influenza viruses are susceptible to infection of these viruses, and thus may serve as a mediator of inter-species transmission of IAVs between human and avian populations. In Taiwan, a large-scale outbreak of low pathogenic avian influenza (LPAI) H5 viruses occurred in 2003 causing great economic loss. Furthermore, the 2009 emerged triple-reassorted pandemic H1N1 viruses (pH1N1/09) with swine- and avian-origin gene segments rapidly spread human-to-human populations leading to pandemics. Therefore, the specific aims of this study were to investigate possible inter-species transmission of LPAI H5 and the pH1N1/09 viruses among economic swine and animal-related workers in Taiwan through serological surveillance and to search for the risk and protective factors for the infections of these two animal-origin influenza viruses.
To approach above issues, this study involved three parts: (1) to conduct a serological surveillance of the pH1N1/09 and LPAI H5 influenza in 846 pigs in County A of central Taiwan from August 2008 to May 2010 (2) to find out the likelihood in acquiring the two viral infections among 1,354 animal-related workers in County A in 2010 by measuring their antibody serotiters; and (3) to investigate factors associated with the two viral infections in these two different host populations, particularly environmental conditions that may reflect local geographical differences in seroprevalence rates of pH1N1/09.
To investigate the epidemiological importance of inter-species transmission in central Taiwan, both 846 swine serum samples (60 farms) from 2008 to 2010, and 1354 human sera from animal-related workers in 2010 were collected in County A. These samples were screened by modified hemagglutinin inhibition (HI) assays using turkey RBCs and the California/7/2009 (H1N1) vaccine strain for measuring anti- pH1N1/09 HI antibody, and the titers >1:40 regarded as seropositive. On the other hand, horse red blood cells (RBCs) and the locally Taiwanese low pathogenic avian influenza (LPAI) H5N2 viruses (Duck/Taiwan/DV1237/2008, isolated from ducks in County A) were used to measure anti-H5 HI antibody, and serotitiers >1:20 determined as seropositive. Risk and protective factors for acquiring both infections in swine and animal-related human populations were further analyzed by univariate and multivariate analyses.
The overall seroprevalence rates of anti-pH1N1/09 in swine populations and swine farms were 19.1% (162/846) and 51.7% (31/60), respectively; with significant increase in 2010 [40.0% (132/330 samples); 78.3% (18/23 farms)] compared to those in 2008 [8.9% (20/225 samples); 53.3%, (8/15 farms)] and in 2009 [3.4%, (10/291 samples); 22.7%, (5/22 farms)] (p<0.0001). These overall seroprevalence rates of the 2009 novel influenza virus in swine were significantly higher than those of LPAI H5 [0.12% (1/846 samples); 1.7% (1/60 farms), (p<0.0001)]. Similar trends in significant differences between these two animal-originated viruses also occurred for pH1N1/09 infection in animal-related workers [21.4% (290/1,354) in all workers and 16.4% (138/841) in non-pH1N1/09 vaccinated workers on pH1N1/09 infection, versus 1.8% (24/1,354) on LPAI H5, p<0.0001].
Multivariate analysis after controlling the study year shows that the risk factor for swine to acquire the pH1N1/09 infection during the past three years was raised swine along the coast [Odds Ratio (OR)=2.33, 95% confidence interval (CI)=1.51 -3.59, p=0.0001], whereas the protective factor was appropriate swine farm management (OR=0.99, 95% CI=0.98-0.995, p=0.0006). The risk and protective factors in the 2010’s pH1N1/09 infection in swine remained the same [raised along the coast (OR=3.43, 95% CI=1.71-6.88, p=0.0005) and well management (OR=0.96, 95% CI=0.95-0.97, p<0.0001)], in addition to another risk factor of the farrow-to-finish raised farm type (OR=2.88, 95% CI=1.45-5.72, p=0.0025).
Regarding to human infection, after controlling age and receiving the pH1N1/09 vaccine, the multivariate analysis reveal that the only statistically significant risk factor for acquiring the 2009 pH1N1 infection among animal-related workers was swine-related labor (OR=1.50, 95% CI=1.11-2.02, p=0.0084), whereas the protective factors were the low-risk occupations [farm’s owners (OR=0.071, 95% CI=0.50-0.99, p=0.042) and slaughters or sellers (OR=0.32, 95% CI=0.14 -0.73, p=0.0061)]. Among those pH1N1/09-unvaccinated workers, the high-risk occupations increased the risk of acquiring this infection [swine farm’s employees (OR=1.62, 95% CI=1.06-2.47, p=0.0257) and veterinarians (OR=4.72, 95% CI=1.51-14.83, p=0.0078)] in contrast, avian-related labors (OR=0.64, 95% CI=0.43-0.96, p=0.0299) and higher body mass index (BMI) (OR=0.91, 95% CI=0.86-0.97, p=0.003) were protective factors. On the other hand, the only risk factor for acquiring the LPAI H5 infection among animal-related workers after controlling age was avian-related labors (OR=3.40, 95% CI=1.21-9.56, p=0.0205), whereas the only protective factor was living in areas with higher densities of pig houses (OR=0.28, 95% CI=0.11-0.76, p=0.0121).
In conclusion, swine populations did strikingly increase the infection of pH1N1/09 in central Taiwan in 2010 after the occurrence of the 2009 pandemic in human in 2009. On the contrary, LPAI H5 virus isolated in County A that had not been adapted to swine populations yet leading that the seroprevalenc of this H5 virus infection was extremely low in animal-related workers. This first seroepidemiological study in both swine and swine workers in the same county can provide us more clues on inter-species transmission of important novel influenza viruses in this island where poultry density ranked the highest. Since Taiwan has been the HPAI-free area domestically and has not had outbreaks of novel influenza among human or swine populations, virological and serological surveillance to detect novel influenza viruses in farms and high risk populations with animal exposures in the countryside should be reinforced continuously. In addition, future research needs to focus on serological surveillance of influenza viruses among paired animal-related workers and their farm animals and investigating the mechanism involved in novel influenza viruses to become selection advantageous viruses for replacing the localized animal influenza viruses.

参考文献 ( 121 ) 〈TOP〉

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使用DOI作为永久连结

引用含有DOI的文献

DOI可强化引用精确性、增强学术圈连结，并给予使用者跨平台的良好使用经验，目前在全世界已有超过五千万个对象申请DOI。 如想对DOI的使用与概念有进一步了解，请参考 （ ） 。

DOI可强化引用精确性、增强学术圈连结，并给予使用者跨平台的良好使用经验，目前在全世界已有超过五千万个对象申请DOI。如想对DOI的使用与概念有进一步了解，请参考（）。