Journal of Medical Virology 86:592–596 (2014)
Antibodies Against Avian-Like A (H1N1) Swine Influenza Virus Among Swine Farm Residents in Eastern China Xiuchen Yin,1 Xin Yin,2 Baizhong Rao,1 Chunfang Xie,1 Pengchao Zhang,1 Xian Qi,3 Ping Wei,2 and Huili Liu1* 1
Institute of Animal Science and Veterinary Medicine, Shanghai Academy of Agricultural Sciences, Shanghai Municipal Key Laboratory of Agri-genetics and Breedings, Shanghai, China 2 Northeast Agricultural University, College of Veterinary Medicine, Haerbin, Heilongjiang Province, China 3 Jiangsu Center for Disease Control and Prevention, Nan Jing, Jiangsu Province, China
In 2007, the avian-like H1N1 virus (A/swine/ Zhejiang/1/07) was first isolated in pigs in China. Recently, it was reported that a 3-yearold boy was infected with avian-like A (H1N1) swine influenza virus (SIV) in Jiangsu Province, China. To investigate the prevalence of avianlike A (H1N1) SIV infection among swine farm residents in eastern China, an active influenza surveillance program was conducted on swine farms in this region from May 21, 2010 through April 22, 2012. A total of 1,162 participants were enrolled, including 1,136 persons from 48 pig farms, as well as 26 pig farm veterinarians. A total of 10.7% and 7.8% swine farm residents were positive for antibodies against avian-like A (H1N1) SIV by HI and NT assay, respectively, using 40 as the cut-off antibody titer. Meanwhile, all the serum samples collected from a control of healthy city residents were negative against avian-like A (H1N1) SIV. As the difference in numbers of antibody positive samples between the swine farm residents and health city residents controls was statistically significant (P ¼ 0.002), these data suggest that occupational exposure to pigs may increase swine farm residents’ and veterinarians’ risk of avianlike A (H1N1) SIV infection in eastern China. This study provides the first data on avian-like A (H1N1) SIV infections in humans in China; the potential for avian-like A (H1N1) SIV entering the human population should also be taken into consideration. J. Med. Virol. 86:592– 596, 2014. # 2013 Wiley Periodicals, Inc. KEY WORDS:
swine influenza viruses; avianlike A (H1N1); swine farm residents
C 2013 WILEY PERIODICALS, INC.
INTRODUCTION Influenza A viruses are known to infect a wide variety of animals. Studies have repeatedly shown that the influenza A virus can shift from one species to another. In particular, influenza is a highly contagious and economically important cause of respiratory disease in pigs worldwide [Easterday and Hinshaw, 1992; Su et al., 2013a]. H1N1 is one of the main subtypes of influenza virus currently circulating in both human and swine populations worldwide. Circulating swine influenza viruses (SIVs) are associated with the classical swine (CS) lineage, the Eurasian avian-like (EA) lineage, and the North American triple reassortant (TR) lineage [Brown, 2000]. In recent years, surveys of H1N1 SIV infection have been reported worldwide [Kendal et al., 1982; Gibbs et al., 2009; Liu et al., 2009; Yu et al., 2009; Zhu et al., 2011]. The Eurasian avianlike A (H1N1) SIV has circulated in pigs in some (not all) European and Asian countries since 1979. H1N1 SIVs with avian-like HA genes rarely infect humans, and the human population would likely be immunologically naive to such a virus [Liu et al., 2009] In 2007, the avian-like H1N1 virus (A/swine/Zhejiang/1/ 07) was first isolated in pigs in China. Recently, it
Grant sponsor: Shanghai Agricultural Commission Key Project; Grant number: 2009-5-2. Conflicts of interest: None. Correspondence to: Huili Liu, Institute of Animal Science and Veterinary Medicine, Shanghai Academy of Agricultural Sciences, Shanghai Municipal Key Laboratory of Agri-genetics and Breedings, Shanghai 201106, China. E-mail: [email protected] Accepted 8 October 2013 DOI 10.1002/jmv.23842 Published online 8 November 2013 in Wiley Online Library (wileyonlinelibrary.com).
Antibodies Against Avian Like H1N1 Swine Influenza Virus
was reported that a 3-year-old boy was infected with an avian-like A (H1N1) SIV in Jiangsu Province, China [Yu et al., 2009]. These cases suggest risk of transmission of avian-like A (H1N1) SIV in persons who have direct exposure to pigs; however, to date, no serological studies about avian-like A (H1N1) SIV infections have been carried out in swine farm residents in China. This study was initiated to serologically assess the relative risk of exposure to avian-like A (H1N1) SIVs among people involved in swine farming. Possibly due to the special geographical and climatic conditions, and especially the high densities of humans and animals in close contact in eastern China, many novel pandemic influenza viruses might be generated here and spread to other areas. Because a relatively small number of zoonotic avian-like A (H1N1) SIV infections have been documented by virus isolation, whether infections with avian-like A (H1N1) SIV are clinically different from infections with pandemic (H1N1) 2009 virus remains unclear. Early prevention and detection will be an important component of a pandemic preparedness plan; therefore, the potential for avian-like A (H1N1) SIV entering the human population should also be taken into account. MATERIALS AND METHODS To investigate the prevalence of avian-like A (H1N1) SIV infection among swine farm residents in China, an active influenza surveillance program was conducted on swine farms in this region from May 21, 2011 through April 22, 2012 (Fig. 1). Detailed information about the swine farm residents living in rural areas of eastern China, including names and corresponding contacts, was provided by local veterinarians. The farm residents were tele-
Fig. 1. Survey sites in eastern China where the surveillance was conducted.
593
phone contacted to inquire about the possibility of attending the project. The participants were asked to provide necessary information, such as their general health condition and the nature of their contact with pigs. Other possible employees on the swine farm and farm veterinarians were also included in the project. In total, 1,162 persons were registered; 1,136 participants were from 48 pig farms and 26 participants were swine farm veterinarians. Peripheral blood samples (5 ml each) were obtained by trained healthcare workers. Participants’ sera were stored at 20˚C until use. As a control, 104 serum samples were collected from unvaccinated healthy city residents in Nanchang, the capital city of Jiangxi. None of the participants had been vaccinated by seasonal influenza or pandemic (H1N1) 2009 virus vaccines. The induced cross-reactive immunization with seasonal influenza vaccine or pandemic 2009 H1N1 vaccine antibody response to avian-like A (H1N1) SIV and PDM-09 can be ignored. To detect the samples without divulging personal identities, each sample was assigned at random an ID number. This study’s protocol was reviewed and approved by the Institutional Review Board at the Jiangsu Center for Disease Control and Prevention. An informed consent was provided and signed by each participant. Previous results show that little cross-reactivity exists between the pandemic (H1N1) 2009 virus and the avian-like A (H1N1) SIVs subtype viruses [Yu et al., 2009; Zhu et al., 2011]. Influenza viruses used in this study were A/California/7/2009 [pandemic (H1N1) 2009 virus] and A/swine/Zhejiang/1/07 [Avian-like A (H1N1) SIV]. These influenza viruses were provided by the Institute of Animal Science and Veterinary Medicine, Shanghai, Shanghai Academy of Agricultural Sciences. To eliminate the nonspecific inhibitor in human serum, each serum sample was pre-treated with a 1:5 (v/v) of receptor destroying enzyme (RDE, prepared by Chinese National Influenza Center) at 37˚C for 18 hr, and then incubated at 56˚C for 1 hr to inactivate RDE. The adsorbed serum was carefully removed without disturbing packed cells and used in the HI assay. Briefly, twofold serial dilutions of serum samples were added in V-shaped microtiter plate and 4 HA units of virus were added to each well. The mixture was incubated at room temperature for 35 min. Then, 0.5% (v/v) chicken red blood cells (RBCs) were added to each well. The plates were left at room temperature for 40 min. The HI titers are expressed as the highest dilution of serum giving complete inhibition of agglutination. A sample was considered seropositive when the HI titer 40 [Kendal et al., 1982]. The NT test was used in parallel with the HI test to detect HA subtype-specific antibodies to the avianlike A (H1N1) SIV in the participant sera in this study [Kitikoon et al., 2011]. Serial dilutions of RDEtreated serum samples were mixed with 100 TCID50 of the virus and incubated at 37˚C for 1 hr. The virus J. Med. Virol. DOI 10.1002/jmv
594
Yin et al.
and serum mixtures were inoculated onto confluent MDCK cell monolayers in 96-well plates, and incubated at 37˚C in 5% CO2. After 1 hr, the inoculum was removed and 100 ml of MEM was added to each well. Cells were incubated at 35˚C for 2 days. The NT titers were determined as the reciprocal of the serum dilution that caused 50% inhibition of the cytopathic effect. NT titer 40 are considered seropositive and indicate previous infection [Olsen et al., 2002]. SPSS for Windows version (Release 17.0 standard version, SPSS, Inc., Chicago, IL) was used for all statistical analyses. The chi-square test was used and statistical significance was defined as P < 0.05. RESULTS The total numbers of volunteers participating in the current study were 432, 306, and 424 from Jiangsu, Zhejiang, and Fujian, respectively (Table I). Among the 1,162 participants, 793 participants were swine farm employees and their average occupational age was 14.7 years. Conversely, participants from the Jiangxi control group were from schools and small factories. Most participants from Jiangsu, Zhejiang, and Fujian were directly exposed to pigs around their household, and pigs represented the most frequently contacted species. Screening all 1,162 serum samples with A/California/7/2009 showed that 502 (43.2%) samples had HI titers > 40 (Table II). A total of 10.7% (124/1,162) and 7.8% (91/1,162) swine farm residents were positive for antibodies against A/swine/Zhejiang/1/07 by HI and NT assay, respectively, using 40 as a cut-off antibody titer. Ninety-one serum samples that were NT positive for A/swine/Zhejiang/1/07 were also HI positive, and all the seropositive serum samples were from swine farm workers and veterinarian. Fourteen
of the positive samples were female and thirty of the positive samples had reactivity towards pandemic (H1N1) 2009 (Table III). The anti-avian-like H1N1 SIV-positive rate was also significantly higher among men workers than women workers (9.1% vs. 4.4%, P ¼ 0.041). Based on the questionnaire, age, geographic location, and history of pigs contact were all not statistically associated with avian-like A (H1N1) SIV infection (P > 0.05). The 104 serum samples from Jiangxi had no hemagglutination inhibition antibodies against A/swine/Zhejiang/1/07, but the control group had 33% seropositve rates for A/California/7/ 2009 (Table II). The difference in numbers of avianlike A (H1N1) SIV antibody positive samples between the swine farm residents and healthy city residents controls was statistically significant (P ¼ 0.002). DISCUSSION Epidemiological and serological evidence have indicated that swine farm residents are high-risk groups [Ayora-Talavera et al., 2005; Kitikoon et al., 2011]. Due to the nature of their work environment and practices, swine farm residents are also at high risk of exposure to SIV. In eastern China, apart from this report, no information about the prevalence of antibodies to avian-like A (H1N1) SIV in swine farm residents exists. A total of 10.7% (124/1,162) sera samples were found positive by using HI test in swine farm residents in eastern China. A significant difference (P ¼ 0.002) was observed between the numbers of positive samples among the controls and the farm residents. The difference in numbers of avianlike A (H1N1) SIV antibody positive samples between the swine farm residents and healthy city residents controls was statistically significant (P ¼ 0.002). These data suggest that occupational exposure to
TABLE I. Geographic Areas and Groups Surveyed in Southeastern China Where the Seroepidemiological Study Was Conducted No. demographic description Locationsa
No.
Median of age (range)
No. of female (%)
Jiangsua
432
42 (8–80)
106 (24.54)
Zhejianga
306
46 (11–72)
92 (30.06)
Fujiana
424
39 (10–75)
119 (28.07)
Jiangxib
104
31 (9–87)
49 (47.12)
a
Occupation (average occupational age) Swine farm veterinarian Farm owners Swine farm workers Spouses and children Swine farm veterinarian Farm owners Swine farm workers Spouses and children Swine farm veterinarian Farm owners Swine farm workers Spouses and children Students Teachers Industrial workers
10 (13.22) 22 (18.29) 297 (12.5) 103 11 (9.74) 11 (19.91) 200 (15.6) 84 9 (16.12) 14 (23.31) 296 (16.3) 105 58 23 23
Survey sites in southeastern China where the seroepidemiological study was conducted. Control serum samples were collected from unvaccinated healthy city residents in Nanchang, the capital city of Jiangxi Province.
b
J. Med. Virol. DOI 10.1002/jmv
Antibodies Against Avian Like H1N1 Swine Influenza Virus
595
TABLE II. Serologic Results in Southeastern China. Jiangsu (432) Virus, titer
HI
Zhejiang (306) NT
HI
Fujian (424) NT
Pandemic (H1N1) 2009 virus A/California/7/2009 40–80 169 82 160 21 19 101 (101 0.58)a Total 190 (189.67 2.03)a Positive rate (%) 43.98 33.01 Avian-like A (H1N1) swine influenza virus A/swine/Zhejiang/1/07 40–80 32 23b 41 24b 6 3b 160 12 11b 34 47 (48.33 1.33)a 27 Total 44 (43.14 0.33)a Positive rate (%) 10.20 15.36
HI
Jiangxi (104) NT
183 28 211 (214.33 3.84)a 49.76 29 4 33 (34.33 0.33)a 7.78
HI
NT
26 7 33 (33.67 0.67)a 31.73 26b 4b 30
0 0 0 (0)a
0 0 0
a Calculate the 95 percent confidence limits with the formulas: Mean 1.96 Standard Error and Mean þ 1.96 Standard Error for the leftand right-hand side confidence limits. b All the NT positive serum samples were also HI positive.
pigs may increase swine farm residents’ and veterinarians’ risk of avian-like A (H1N1) SIV infection in eastern China. Swine production industries in southeastern China are different from European and North American industries. The production size of swine farm in eastern China ranges from large-scale swine farms (>3,000 pigs) to backyard farms (
Antibodies Against Avian-Like A (H1N1) Swine Influenza Virus Among Swine Farm Residents in Eastern China Xiuchen Yin,1 Xin Yin,2 Baizhong Rao,1 Chunfang Xie,1 Pengchao Zhang,1 Xian Qi,3 Ping Wei,2 and Huili Liu1* 1
Institute of Animal Science and Veterinary Medicine, Shanghai Academy of Agricultural Sciences, Shanghai Municipal Key Laboratory of Agri-genetics and Breedings, Shanghai, China 2 Northeast Agricultural University, College of Veterinary Medicine, Haerbin, Heilongjiang Province, China 3 Jiangsu Center for Disease Control and Prevention, Nan Jing, Jiangsu Province, China
In 2007, the avian-like H1N1 virus (A/swine/ Zhejiang/1/07) was first isolated in pigs in China. Recently, it was reported that a 3-yearold boy was infected with avian-like A (H1N1) swine influenza virus (SIV) in Jiangsu Province, China. To investigate the prevalence of avianlike A (H1N1) SIV infection among swine farm residents in eastern China, an active influenza surveillance program was conducted on swine farms in this region from May 21, 2010 through April 22, 2012. A total of 1,162 participants were enrolled, including 1,136 persons from 48 pig farms, as well as 26 pig farm veterinarians. A total of 10.7% and 7.8% swine farm residents were positive for antibodies against avian-like A (H1N1) SIV by HI and NT assay, respectively, using 40 as the cut-off antibody titer. Meanwhile, all the serum samples collected from a control of healthy city residents were negative against avian-like A (H1N1) SIV. As the difference in numbers of antibody positive samples between the swine farm residents and health city residents controls was statistically significant (P ¼ 0.002), these data suggest that occupational exposure to pigs may increase swine farm residents’ and veterinarians’ risk of avianlike A (H1N1) SIV infection in eastern China. This study provides the first data on avian-like A (H1N1) SIV infections in humans in China; the potential for avian-like A (H1N1) SIV entering the human population should also be taken into consideration. J. Med. Virol. 86:592– 596, 2014. # 2013 Wiley Periodicals, Inc. KEY WORDS:
swine influenza viruses; avianlike A (H1N1); swine farm residents
C 2013 WILEY PERIODICALS, INC.
INTRODUCTION Influenza A viruses are known to infect a wide variety of animals. Studies have repeatedly shown that the influenza A virus can shift from one species to another. In particular, influenza is a highly contagious and economically important cause of respiratory disease in pigs worldwide [Easterday and Hinshaw, 1992; Su et al., 2013a]. H1N1 is one of the main subtypes of influenza virus currently circulating in both human and swine populations worldwide. Circulating swine influenza viruses (SIVs) are associated with the classical swine (CS) lineage, the Eurasian avian-like (EA) lineage, and the North American triple reassortant (TR) lineage [Brown, 2000]. In recent years, surveys of H1N1 SIV infection have been reported worldwide [Kendal et al., 1982; Gibbs et al., 2009; Liu et al., 2009; Yu et al., 2009; Zhu et al., 2011]. The Eurasian avianlike A (H1N1) SIV has circulated in pigs in some (not all) European and Asian countries since 1979. H1N1 SIVs with avian-like HA genes rarely infect humans, and the human population would likely be immunologically naive to such a virus [Liu et al., 2009] In 2007, the avian-like H1N1 virus (A/swine/Zhejiang/1/ 07) was first isolated in pigs in China. Recently, it
Grant sponsor: Shanghai Agricultural Commission Key Project; Grant number: 2009-5-2. Conflicts of interest: None. Correspondence to: Huili Liu, Institute of Animal Science and Veterinary Medicine, Shanghai Academy of Agricultural Sciences, Shanghai Municipal Key Laboratory of Agri-genetics and Breedings, Shanghai 201106, China. E-mail: [email protected] Accepted 8 October 2013 DOI 10.1002/jmv.23842 Published online 8 November 2013 in Wiley Online Library (wileyonlinelibrary.com).
Antibodies Against Avian Like H1N1 Swine Influenza Virus
was reported that a 3-year-old boy was infected with an avian-like A (H1N1) SIV in Jiangsu Province, China [Yu et al., 2009]. These cases suggest risk of transmission of avian-like A (H1N1) SIV in persons who have direct exposure to pigs; however, to date, no serological studies about avian-like A (H1N1) SIV infections have been carried out in swine farm residents in China. This study was initiated to serologically assess the relative risk of exposure to avian-like A (H1N1) SIVs among people involved in swine farming. Possibly due to the special geographical and climatic conditions, and especially the high densities of humans and animals in close contact in eastern China, many novel pandemic influenza viruses might be generated here and spread to other areas. Because a relatively small number of zoonotic avian-like A (H1N1) SIV infections have been documented by virus isolation, whether infections with avian-like A (H1N1) SIV are clinically different from infections with pandemic (H1N1) 2009 virus remains unclear. Early prevention and detection will be an important component of a pandemic preparedness plan; therefore, the potential for avian-like A (H1N1) SIV entering the human population should also be taken into account. MATERIALS AND METHODS To investigate the prevalence of avian-like A (H1N1) SIV infection among swine farm residents in China, an active influenza surveillance program was conducted on swine farms in this region from May 21, 2011 through April 22, 2012 (Fig. 1). Detailed information about the swine farm residents living in rural areas of eastern China, including names and corresponding contacts, was provided by local veterinarians. The farm residents were tele-
Fig. 1. Survey sites in eastern China where the surveillance was conducted.
593
phone contacted to inquire about the possibility of attending the project. The participants were asked to provide necessary information, such as their general health condition and the nature of their contact with pigs. Other possible employees on the swine farm and farm veterinarians were also included in the project. In total, 1,162 persons were registered; 1,136 participants were from 48 pig farms and 26 participants were swine farm veterinarians. Peripheral blood samples (5 ml each) were obtained by trained healthcare workers. Participants’ sera were stored at 20˚C until use. As a control, 104 serum samples were collected from unvaccinated healthy city residents in Nanchang, the capital city of Jiangxi. None of the participants had been vaccinated by seasonal influenza or pandemic (H1N1) 2009 virus vaccines. The induced cross-reactive immunization with seasonal influenza vaccine or pandemic 2009 H1N1 vaccine antibody response to avian-like A (H1N1) SIV and PDM-09 can be ignored. To detect the samples without divulging personal identities, each sample was assigned at random an ID number. This study’s protocol was reviewed and approved by the Institutional Review Board at the Jiangsu Center for Disease Control and Prevention. An informed consent was provided and signed by each participant. Previous results show that little cross-reactivity exists between the pandemic (H1N1) 2009 virus and the avian-like A (H1N1) SIVs subtype viruses [Yu et al., 2009; Zhu et al., 2011]. Influenza viruses used in this study were A/California/7/2009 [pandemic (H1N1) 2009 virus] and A/swine/Zhejiang/1/07 [Avian-like A (H1N1) SIV]. These influenza viruses were provided by the Institute of Animal Science and Veterinary Medicine, Shanghai, Shanghai Academy of Agricultural Sciences. To eliminate the nonspecific inhibitor in human serum, each serum sample was pre-treated with a 1:5 (v/v) of receptor destroying enzyme (RDE, prepared by Chinese National Influenza Center) at 37˚C for 18 hr, and then incubated at 56˚C for 1 hr to inactivate RDE. The adsorbed serum was carefully removed without disturbing packed cells and used in the HI assay. Briefly, twofold serial dilutions of serum samples were added in V-shaped microtiter plate and 4 HA units of virus were added to each well. The mixture was incubated at room temperature for 35 min. Then, 0.5% (v/v) chicken red blood cells (RBCs) were added to each well. The plates were left at room temperature for 40 min. The HI titers are expressed as the highest dilution of serum giving complete inhibition of agglutination. A sample was considered seropositive when the HI titer 40 [Kendal et al., 1982]. The NT test was used in parallel with the HI test to detect HA subtype-specific antibodies to the avianlike A (H1N1) SIV in the participant sera in this study [Kitikoon et al., 2011]. Serial dilutions of RDEtreated serum samples were mixed with 100 TCID50 of the virus and incubated at 37˚C for 1 hr. The virus J. Med. Virol. DOI 10.1002/jmv
594
Yin et al.
and serum mixtures were inoculated onto confluent MDCK cell monolayers in 96-well plates, and incubated at 37˚C in 5% CO2. After 1 hr, the inoculum was removed and 100 ml of MEM was added to each well. Cells were incubated at 35˚C for 2 days. The NT titers were determined as the reciprocal of the serum dilution that caused 50% inhibition of the cytopathic effect. NT titer 40 are considered seropositive and indicate previous infection [Olsen et al., 2002]. SPSS for Windows version (Release 17.0 standard version, SPSS, Inc., Chicago, IL) was used for all statistical analyses. The chi-square test was used and statistical significance was defined as P < 0.05. RESULTS The total numbers of volunteers participating in the current study were 432, 306, and 424 from Jiangsu, Zhejiang, and Fujian, respectively (Table I). Among the 1,162 participants, 793 participants were swine farm employees and their average occupational age was 14.7 years. Conversely, participants from the Jiangxi control group were from schools and small factories. Most participants from Jiangsu, Zhejiang, and Fujian were directly exposed to pigs around their household, and pigs represented the most frequently contacted species. Screening all 1,162 serum samples with A/California/7/2009 showed that 502 (43.2%) samples had HI titers > 40 (Table II). A total of 10.7% (124/1,162) and 7.8% (91/1,162) swine farm residents were positive for antibodies against A/swine/Zhejiang/1/07 by HI and NT assay, respectively, using 40 as a cut-off antibody titer. Ninety-one serum samples that were NT positive for A/swine/Zhejiang/1/07 were also HI positive, and all the seropositive serum samples were from swine farm workers and veterinarian. Fourteen
of the positive samples were female and thirty of the positive samples had reactivity towards pandemic (H1N1) 2009 (Table III). The anti-avian-like H1N1 SIV-positive rate was also significantly higher among men workers than women workers (9.1% vs. 4.4%, P ¼ 0.041). Based on the questionnaire, age, geographic location, and history of pigs contact were all not statistically associated with avian-like A (H1N1) SIV infection (P > 0.05). The 104 serum samples from Jiangxi had no hemagglutination inhibition antibodies against A/swine/Zhejiang/1/07, but the control group had 33% seropositve rates for A/California/7/ 2009 (Table II). The difference in numbers of avianlike A (H1N1) SIV antibody positive samples between the swine farm residents and healthy city residents controls was statistically significant (P ¼ 0.002). DISCUSSION Epidemiological and serological evidence have indicated that swine farm residents are high-risk groups [Ayora-Talavera et al., 2005; Kitikoon et al., 2011]. Due to the nature of their work environment and practices, swine farm residents are also at high risk of exposure to SIV. In eastern China, apart from this report, no information about the prevalence of antibodies to avian-like A (H1N1) SIV in swine farm residents exists. A total of 10.7% (124/1,162) sera samples were found positive by using HI test in swine farm residents in eastern China. A significant difference (P ¼ 0.002) was observed between the numbers of positive samples among the controls and the farm residents. The difference in numbers of avianlike A (H1N1) SIV antibody positive samples between the swine farm residents and healthy city residents controls was statistically significant (P ¼ 0.002). These data suggest that occupational exposure to
TABLE I. Geographic Areas and Groups Surveyed in Southeastern China Where the Seroepidemiological Study Was Conducted No. demographic description Locationsa
No.
Median of age (range)
No. of female (%)
Jiangsua
432
42 (8–80)
106 (24.54)
Zhejianga
306
46 (11–72)
92 (30.06)
Fujiana
424
39 (10–75)
119 (28.07)
Jiangxib
104
31 (9–87)
49 (47.12)
a
Occupation (average occupational age) Swine farm veterinarian Farm owners Swine farm workers Spouses and children Swine farm veterinarian Farm owners Swine farm workers Spouses and children Swine farm veterinarian Farm owners Swine farm workers Spouses and children Students Teachers Industrial workers
10 (13.22) 22 (18.29) 297 (12.5) 103 11 (9.74) 11 (19.91) 200 (15.6) 84 9 (16.12) 14 (23.31) 296 (16.3) 105 58 23 23
Survey sites in southeastern China where the seroepidemiological study was conducted. Control serum samples were collected from unvaccinated healthy city residents in Nanchang, the capital city of Jiangxi Province.
b
J. Med. Virol. DOI 10.1002/jmv
Antibodies Against Avian Like H1N1 Swine Influenza Virus
595
TABLE II. Serologic Results in Southeastern China. Jiangsu (432) Virus, titer
HI
Zhejiang (306) NT
HI
Fujian (424) NT
Pandemic (H1N1) 2009 virus A/California/7/2009 40–80 169 82 160 21 19 101 (101 0.58)a Total 190 (189.67 2.03)a Positive rate (%) 43.98 33.01 Avian-like A (H1N1) swine influenza virus A/swine/Zhejiang/1/07 40–80 32 23b 41 24b 6 3b 160 12 11b 34 47 (48.33 1.33)a 27 Total 44 (43.14 0.33)a Positive rate (%) 10.20 15.36
HI
Jiangxi (104) NT
183 28 211 (214.33 3.84)a 49.76 29 4 33 (34.33 0.33)a 7.78
HI
NT
26 7 33 (33.67 0.67)a 31.73 26b 4b 30
0 0 0 (0)a
0 0 0
a Calculate the 95 percent confidence limits with the formulas: Mean 1.96 Standard Error and Mean þ 1.96 Standard Error for the leftand right-hand side confidence limits. b All the NT positive serum samples were also HI positive.
pigs may increase swine farm residents’ and veterinarians’ risk of avian-like A (H1N1) SIV infection in eastern China. Swine production industries in southeastern China are different from European and North American industries. The production size of swine farm in eastern China ranges from large-scale swine farms (>3,000 pigs) to backyard farms (
