Serological report of pandemic (H1N1) 2009 infection among cats in Northeastern China in 2012-02 and 2013-03
- Fu-Rong Zhao†1,
- Chun-Guo Liu†1, 2, 3,
- Xin Yin1, 2, 3,
- Dong-Hui Zhou1,
- Ping Wei1, 3Email author and
- Hui-Yun Chang1Email author
© Zhao et al.; licensee BioMed Central Ltd. 2014
Received: 25 November 2013
Accepted: 4 March 2014
Published: 14 March 2014
Influenza A virus has a wide range of hosts. It has not only infected human, but also been reported interspecies transmission from humans to other animals, such as pigs, poultry, dogs and cats. However, prevalence of A (H1N1) pdm09 influenza virus infections in cats in northeastern China is unknown. Therefore, the prevalence of A (H1N1) pdm09 influenza virus infections was performed among cats in northeastern China in this study.
Of all samples in this study, the overall seroprevalence of pandemic (H1N1) 2009 infection in cats was 21% (240/1140). It also showed a higher prevalence rate of pandemic(H1N1) 2009 infection in pet cats (30.6%) than roaming cats (11%) based on NT. In addition, the results also showed a trend of difference in term of species of cats and it was statistically significant.
This is the first survey on the seroprevalence of pandemic (H1N1) 2009 infection among cats in northeastern China. This study has observed a relatively high seroprevalence of pandemic (H1N1) 2009 among different cat populations in northeastern China, similar seroprevalence studies should be conducted elsewhere.
KeywordsPandemic (H1N1) 2009 Cats Serological
Influenza A virus has a wide range of hosts. Often the susceptibility of the species is dependent upon the characteristics of the virus and host. Numerous subtypes of influenza A viruses, including influenza A pandemic H1N1 2009 virus, have been shown to cross-species transmission. Since 2009, a novel influenza A virus (H1N1), now called A (H1N1) pdm09 influenza virus, has caused human influenza outbreaks in North America  and a worldwide pandemic [2–4]. To date, it has not only infected human, but also been reported interspecies transmission from humans to other animals, such as pigs, poultry, dogs [5–7].
Recently, the reports have shown that cats can also infected A (H1N1) pdm09 influenza virus [5, 8]. Due to frequent cohabitation and close contacts with humans and other animals, cats are uniquely positioned to serve as reservoirs for influenza virus infection both within a household and within the larger farm or rural environment in China [9, 10]. However, prevalence of A (H1N1) pdm09 influenza virus infection in cats in northeastern China is unknown. Therefore, the prevalence of A (H1N1) pdm09 influenza virus infections was performed among cats in northeastern China in this study.
Seroprevalence of pandemic (H1N1) 2009 in cats in different cities in northeastern China
Seroprevalence of pandemic (H1N1) 2009 in cats of different ages and genders, in northeastern China using the NT and HI assay
Unadjusted OR (95% CI)
Adjusted OR (95% CI)
Less than 4 years
4 years and more
Prevalence of elevated antibody titers against a canine influenza H3N2, a seasonal influenza H1N1, and A(H1N1)pdm09 among cats by hemagglutination inhibition (HI) assay, northeastern China a
HI assay virus
Number of specimens with titers ≥1:40 (%)
Few seroprevalence studies on pandemic (H1N1) 2009 infections have been attempted in cats worldwide. The prevalence of this virus infection in cats in mainland China remains unknown. This is the first survey on the seroprevalence of pandemic (H1N1) 2009 infection in cats in northeastern China. Of all sera from cats in this study, 21% was identified as pandemic (H1N1) 2009 positive. In another conducting the seroprevalence of antibodies against (H1N1) pdm09 among cats in small cities of southern China was only 1.2% in 2011 . Our increased antibody prevalence might be explained a number of ways. Perhaps cats were at a higher probability of infection in northeastern China, due to they exposures in dense populations of humans with high influenza A (H1N1) pdm09 attack rates. The difference might also be explained by the one year temporal difference between cats sampled in southern China in that the northeastern China cats had 1 more years to acquire influenza A (H1N1) pdm09 virus infection. Additionally, the prevalence of seropositive pandemic (H1N1) 2009 in male cats versus female cats suggests that the male cats may be more susceptible (P < 0.05) to the pandemic (H1N1) 2009 infections (Table 2). We hypothesize that relatively high A (H1N1) pdm09 transmission may have occurred between humans and cats during the period of virus infection in the human population. This hypothesis is supported by our observation that pet cats were more likely to have evidence of previous infection with A (H1N1) pdm09 that were roaming cats (30.6% vs11%, P = 0.0032) and also suggests a likely transmission between infected owners and their pets by close contact. Serological evidence of A (H1N1) pdm09 in domestic cats has been reported in the past. In a sero-survey conducted in Italy in 2009, a contrary low prevalence had been observed among dogs, while no cats were reported to have antibodies against A(H1N1)pdm09 in the screen . A similar high prevalence of 21.8% and 22.5% were recorded in a population of cats in the United States, but the study sample comprised animals with a history of respiratory disease . We hypothesized the sustained transmission of the influenza A (H1N1) pdm09 virus in the human population in our study area. In addition, it should be noted that 240 samples from the two small animal shelters in Harbin and Changchun had exposure to pandemic (H1N1) 2009 before sample collection. The higher prevalence of seropositive pandemic A (H1N1) pmd09 among Harbin and Changchun cats versus Shenyang and Dalian is unexplained.
Since cats may be exposed to different influenza virus subtypes, including human-avian and avian-origin influenza viruses, their potential role in the epidemiology of influenza virus should be further investigated. In summary, this study has observed a relatively high seroprevalence of pandemic (H1N1) 2009 in cats in northeastern China, similar seroprevalence studies should be conducted elsewhere. The studies showed that the prevalence for A (H1N1) pdm09 in human was correlated with age and population density. Preexisting antibody may have protected the very old from A (H1N1) pdm09 infection, while original antigenic sin and immunosenescence may have contributed to greater severity once infected [13–15]. Compare with all serum samples collected in 2008 had no HI and NT antibodies against A/California/7/2009, these results reflect the pandemic (H1N1) 2009 had been spread in cats. Concerns of rapid spread in small animal shelters and household may be needed. These observations highlight the need for monitoring cats in pet hospitals and small animal shelters are necessary for us to understand what roles cats plan in the ecology of influenza A virus.
This work was supported by National Transgenic Project of China (2011ZX08011-004), and Basic Conditions for Science and Technology Projects of Lanzhou City (2012-2-71).
- Centers for Disease C, Prevention: Swine influenza A (H1N1) infection in two children--Southern California, March-April 2009. MMWR Morb Mortal Wkly Rep 2009, 58: 400-402.Google Scholar
- Kilbourne ED: Influenza pandemics of the 20th century. Emerg Infect Dis 2006, 12: 9-14. 10.3201/eid1201.051254PubMedPubMed CentralView ArticleGoogle Scholar
- Organization WH: Influenza A (H1N1)—update 48. 2009.http://www.who.int/csr/don/2009_06_12/en/ Available fromGoogle Scholar
- Organization WH: World now at the start of 2009 influenza pandemic. 2009.http://www.who.int/mediacentre/news/statements/2009/h1n1_pandemic_phase6_20090611/en/ Available fromGoogle Scholar
- Sponseller BA, Strait E, Jergens A, Trujillo J, Harmon K, Koster L, Jenkins-Moore M, Killian M, Swenson S, Bender H, Waller K, Miles K, Pearce T, Yoon KJ, Nara P: Influenza A pandemic (H1N1) 2009 virus infection in domestic cat. Emerg Infect Dis 2010, 16: 534-537. 10.3201/eid1603.091737PubMedPubMed CentralView ArticleGoogle Scholar
- Su S, Li HT, Zhao FR, Chen JD, Xie JX, Chen ZM, Huang Z, Hu YM, Zhang MZ, Tan LK, Zhang GH, Li SJ: Avian-origin H3N2 canine influenza virus circulating in farmed dogs in Guangdong, China. Infect Genet Evol 2013, 14: 444-449.PubMedView ArticleGoogle Scholar
- Association AVM: N.Y. dog infected with H1N1; study shows virus non pork. 2010.https://www.avma.org/News/JAVMANews/Pages/100201e.aspx Available fromGoogle Scholar
- Dundon WG, De Benedictis P, Viale E, Capua I: Serologic evidence of pandemic (H1N1) 2009 infection in dogs, Italy. Emerg Infect Dis 2010, 16: 2019-2021. 10.3201/eid1612.100514PubMedPubMed CentralView ArticleGoogle Scholar
- Su S, Qi W, Chen J, Zhu W, Huang Z, Xie J, Zhang G: Seroepidemiological evidence of avian influenza A virus transmission to pigs in southern China. J Clin Microbiol 2013, 51: 601-602. 10.1128/JCM.02625-12PubMedPubMed CentralView ArticleGoogle Scholar
- Ali A, Daniels JB, Zhang Y, Rodriguez-Palacios A, Hayes-Ozello K, Mathes L, Lee CW: Pandemic and seasonal human influenza virus infections in domestic cats: prevalence, association with respiratory disease, and seasonality patterns. J Clin Microbiol 2011, 49: 4101-4105. 10.1128/JCM.05415-11PubMedPubMed CentralView ArticleGoogle Scholar
- Su S, Yuan L, Li H, Chen J, Xie J, Huang Z, Jia K, Li S: Serologic evidence of pandemic influenza virus H1N1 2009 infection in cats in China. Clin Vaccine Immunol 2013, 20: 115-117. 10.1128/CVI.00618-12PubMedPubMed CentralView ArticleGoogle Scholar
- An DJ, Jeoung HY, Jeong W, Chae S, Song DS, Oh JS, Park BK: A serological survey of canine respiratory coronavirus and canine influenza virus in Korean dogs. J Vet Med Sci 2010, 72: 1217-1219. 10.1292/jvms.10-0067PubMedView ArticleGoogle Scholar
- Xu C, Bai T, Iuliano AD, Wang M, Yang L, Wen L, Zeng Y, Li X, Chen T, Wang W, Hu Y, Yang L, Li Z, Zou S, Li D, Wang S, Feng Z, Zhang Y, Yu H, Yang W, Wang Y, Widdowson MA, Shu Y: The seroprevalence of pandemic influenza H1N1 (2009) virus in China. PLoS One 2011,6(4):e17919. 10.1371/journal.pone.0017919PubMedPubMed CentralView ArticleGoogle Scholar
- Zhang X, He J, Li L, Zhu X, Ke C, Ni H, Hou N, Zhong H, Wu J: Serologic survey of the pandemic H1N1 2009 virus in Guangdong Province, China: a cross sectional study. PLoS One 2011,6(8):e23034. 10.1371/journal.pone.0023034PubMedPubMed CentralView ArticleGoogle Scholar
- Liu T, Li Z, Song S, Zhang S, Wang Y, Wang L, Xu A, Wang X, Bi Z: Seroepidemiological study of influenza A (H1N1) pdm09 virus following the 2009-2010 wave in Shandong Province, China. Scand J Infect Dis 2013,45(7):552-556. 10.3109/00365548.2013.793818PubMedView ArticleGoogle Scholar
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