刘开拓;高如一;王晓泉;刘秀梵;

• 1:扬州大学兽医学院农业部畜禽传染病学重点开放实验室
• 2:江苏省动物重要疫病与人兽共患病防控协同创新中心
• 3:江苏省人畜共患病重点实验室

摘要(Abstract)：

禽流感病毒(Avian influenza virus,AIV)不仅严重危害禽类,而且对人类生命健康造成严重威胁。鸽作为留鸟,具有作为AIV从野生鸟类传播至人类中间宿主的潜能。鸽对AIV的易感性以及在病毒传播中的作用却存在争议。通过分析AIV自然感染、人工感染鸽的流行病学以及实验研究数据,同时回顾了禽流感病毒感染鸽的机制,发现随着病毒的进化和时间的推移,鸽群AIV的感染率也在递增;尤其随着近年具有双受体结合特性的高致病性禽流感病毒(highly pathogenic avian influenza virus,HPAIV)clade2.3.4.4分支H5Nx毒株的出现,其感染鸽后排毒量上升以及鸽体间直接接触传播能力增强。为了有效防控AIV的跨种间传播,有必要加强对鸽感染AIV的流行病学监测和传播特性的研究,特别需要密切关注具双受体结合特性的H5Nx和H7N9 HPAIV对鸽易感性的发展趋势。

关键词(KeyWords)： 禽流感病毒;鸽;流行病学;致病性

Abstract:

Keywords:

基金项目(Foundation): 国家重点研发计划（2016YFD05002-1）：动物流感病毒遗传变异与致病机理研究~~

作者(Author): 刘开拓;高如一;王晓泉;刘秀梵;

Email:

DOI: 10.13242/j.cnki.bingduxuebao.003873

参考文献(References)：

• [1]Webster R G,Bean W J,Gorman O T,Chambers TM,Kawaoka Y.Evolution and ecology of influenza Aviruses[J].Microbiol Rev,1992,56(1):152-179.
• [2]Wu Y,Wu Y,Tefsen B,Shi Y,Gao G F.Bat-derived influenza-like viruses H17N10 and H18N11[J].Trends Microbiol,2014,22(4):183-191.
• [3]Long J S,Mistry B,Haslam S M,Barclay W S.Host and viral determinants of influenza A virus species specificity[J].Nat Rev Microbiol,2019,17(2):67-81.
• [4]Xu X,Subbarao K,Cox N J,Guo Y.Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus:similarity of its hemagglutinin gene to those of H5N1 viruses from the1997 outbreaks in Hong Kong[J].Virology,1999,261(1):15-19.
• [5]Yang J R,Liu M T.Human infection caused by an avian influenza A(H7N9)virus with a polybasic cleavage site in Taiwan,2017[J].J Formos Med Assoc,2017,116(3):210-212.
• [6]Olsen B,Munster V J,Wallensten A,Waldenstr?m J,Osterhaus A D,Fouchier R A.Global patterns of influenza a virus in wild birds[J].Science,2006,312(5772):384-388.
• [7]Boon A C,Sandbulte M R,Seiler P,Webby R J,Songserm T,Guan Y,Webster R G.Role of terrestrial wild birds in ecology of influenza A virus(H5N1)[J].Emerg Infect Dis,2007,13(11):1720-1724.
• [8]Perkins L E,Swayne D E.Comparative susceptibility of selected avian and mammalian species to a Hong Kongorigin H5N1 high-pathogenicity avian influenza virus[J].Avian Dis,2003,47(3 Suppl):956-967.
• [9]Barber M R,Aldridge J R,Jr,Webster R G,Magor KE.Association of RIG-I with innate immunity of ducks to influenza[J].Proc Natl Acad Sci U S A,2010,107(13):5913-5918.
• [10]Abolnik C,Stutchbury S,Hartman M J.Experimental infection of racing pigeons (Columba livia domestica)with highly pathogenic Clade 2.3.4.4 sub-group B H5N8avian influenza virus[J].Vet Microbiol,2018,227:127-132.
• [11]Bosco-Lauth A M,Marlenee N L,Hartwig A E,Bowen R A,Root J J.Shedding of clade 2.3.4.4 H5N8and H5N2 highly pathogenic avian influenza viruses in peridomestic wild birds in the U.S[J].Transbound Emerg Dis,2019,66(3):1301-1305.
• [12]Liu K,Gao R,Wang X,Han W,Ji Z,Zheng H,Gu M,Hu J,Liu X,Hu S,Chen S,Gao S,Peng D,Jiao XA,Liu X.Pathogenicity and transmissibility of clade2.3.4.4 highly pathogenic avian influenza virus subtype H5N6 in pigeons[J].Vet Microbiol,2020,247:108776.
• [13]Nettles V F,Wood J M,Webster R G.Wildlife surveillance associated with an outbreak of lethal H5N2avian influenza in domestic poultry[J].Avian Dis,1985,29(3):733-741.
• [14]Z?upan?ic′Z,Ugr?ic′I,Jelavic′V,Ive?a Petri?evic′S,Greguric′J,Jukic′B,Smerdel S.Antibodies for human influenza type A virus in bird sera[J].Veterinarski Arhiv,1986:217-225.
• [15]Motha J,Gibbons A M,Reed C E.A survey for avian paramyxoviruses and influenza viruses in feral pigeons and native birds in New Zealand[J].N Z Vet J,1997,45(5):215-216.
• [16]Guan Y,Shortridge K F,Krauss S,Chin P S,Dyrting K C,Ellis T M,Webster R G,Peiris M.H9N2influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China[J].J Virol,2000,74(20):9372-9380.
• [17]Capua I,Grossele B,Bertoli E,Cordioli P.Monitoring for highly pathogenic avian influenza in wild birds in Italy[J].Vet Rec,2000,147(22):640.
• [18]Liu M,He S,Walker D,Zhou N,Perez D R,Mo B,Li F,Huang X,Webster R G,Webby R J.The influenza virus gene pool in a poultry market in South Central China[J].Virology,2003,305(2):267-275.
• [19]Dovc A,Zorman-Rojs O,Rataj A V,Bole-Hribovsek V,Dobeic M.Health status of free-living pigeons(Columba livia domestica) in the city of Ljubljana[J].Acta Veterinaria Hungarica,2004,52(2):219-226.
• [20]Peroulis I,O′Riley K.Detection of Avian Paramyxoviruses and Influenza viruses amongst wild bird population in Victoria[J].Aust Vet J,2004,82(1-2):79-82.
• [21]Ellis T M,Barry Bousfield R,Bissett L A,Dyrting KC,Luk G S M,Tsim S T,Sturm-ramirez K,Webster R G,Guan Y,Peiris J S M.Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002[J].Avian Pathol,2004,33(5):492-505.
• [22]Khawaja J Z,Naeem K,Ahmed Z,Ahmad S.Surveillance of avian influenza viruses in wild birds in areas adjacent to the epicenter of an outbreak in Federal Capital Territory of Pakistan[J].Int J Poult Sci,2005,4(1):39.
• [23]Lillehaug A,Monceyron Jonassen C,Bergsj?B,Hofshagen M,Tharaldsen J,Nesse L L,Handeland K.Screening of feral pigeon (Colomba livia),mallard(Anas platyrhynchos)and graylag goose(Anser anser)populations for Campylobacter spp.,Salmonella spp.,avian influenza virus and avian paramyxovirus[J].Acta Vet Scand,2005,46(4):193-202.
• [24]Pant G R,Selleck P W.Surveillance for avian influenza in Nepal 2004-2005[J].Avian Dis,51(1 Suppl):352-354.
• [25]Barbour E K,Shaib H A,Rayya E G.Reverse transcriptase-polymerase chain reaction-based surveillance of type A influenza viruses in wild and domestic birds of the Lebanon[J].Vet Ital,2007,43(1):33-41.
• [26]Pérez-Ramírez E,Gerrikagoitia X,Barral M,H?fle U.Detection of low pathogenic avian influenza viruses in wild birds in Castilla-La Mancha(south central Spain)[J].Vet Microbiol,2010,146(3-4):200-208.
• [27]Amonsin A,Choatrakol C,Lapkuntod J,Tantilertcharoen R,Thanawongnuwech R,Suradhat S,Suwannakarn K,Theamboonlers A,Poovorawan Y.Influenza virus (H5N1) in live bird markets and food markets,Thailand[J].Emerg Infect Dis,2008,14(11):1739-1742.
• [28]Kulak M V,Ilinykh F A,Zaykovskaya A V,Epanchinzeva A V,Evstaphiev I L,Tovtunec N N,Sharshov K A,Durimanov A G,Penkovskaya N A,Shestopalov A M.Surveillance and identification of influenza A viruses in wild aquatic birds in the Crimea,Ukraine (2006-2008)[J].Avian Dis,2010,54(3):1086-1090.
• [29]Kohls A,Lüschow D,Lierz M,Hafez H M.Influenza A virus monitoring in urban and free-ranging pigeon populations in Germany,2006-2008[J].Avian Dis,2011,55(3):447-450.
• [30]Zhou J P,Ge F F,Liu J,Ju H B,Yang D Q,Wang J,Zhang W Y,Liu P H.Epidemiological survey and genetic evolution of H9 subtype influenza viruses in Shanghai,China,from 2006 to 2010[J].Arch Virol,2012,157(6):1193-1198.
• [31]Lefran?ois T,Hendrikx P,Ehrhardt N,Millien M,Gomez L,Gouyet L,Gaidet N,Gerbier G,Vachiéry N,Petitclerc F,Carasco-Lacombe C,Pinarello V,Ahoussou S,Levesque A,Gongora H V,Trotman M.Surveillance of avian influenza in the Caribbean through the Caribbean Animal Health Network:surveillance tools and epidemiologic studies[J].Avian Dis,2010,54(1 Suppl):369-373.
• [32]Siengsanan-Lamont J,Robertson I,Blacksell S D,Ellis T,Fenwick S,Saengchoowong S,Suwanpukdee S,Yongyuttawichai P,Sariya L,Prompiram P,Chaichoun K,Wiriyarat W,Pothieng D,Ratanakorn P.Virological and molecular epidemiological investigations into the role of wild birds in the epidemiology of influenza A/H5N1 in central Thailand[J].Vet Microbiol,2011,148(2-4):213-218.
• [33]Dimitrov K M,Manvell R J,Goujgoulova G V.Status of wild birds in Bulgarian zoos with regard to orthomyxovirus and paramyxovirus type 1 infections[J].Avian Dis,2010,54(1 Suppl):361-364.
• [34]Shriner S A,Root J J,Mooers N L,Ellis J W,Stopak S R,Sullivan H J,Van Dalen K K,Franklin A B.Susceptibility of rock doves to low-pathogenic avian influenza A viruses[J].Arch Virol.,2016,161(3):715-720.
• [35]GronesováP,Mi?ákováA,BetákováT.Determination of hemagglutinin and neuraminidase subtypes of avian influenza A viruses in urban pigeons by a new nested RT-PCR[J].Acta Virol,2009,53(3):213-216.
• [36]Nwankwo I O,Faleke O O,Garba J.Avian influenza virus infection in apparently healthy domestic birds in Sokoto,Nigeria[J].Vet Ital,2012,48(3):309-312.
• [37]Mohammadi A,Masoudian M,Nemati Y,Seifi S.Serological and RT-PCR assays for detection of avian influenza of domestic pigeons in Kavar area (Fars province,Iran)[J].Bulg J Vet Med,2010,13(2):117-121.
• [38]Kayali G,El-Shesheny R,Kutkat M A,Kandeil A M,Mostafa A,Ducatez M F,Mc Kenzie P P,Govorkova E A,Nasraa M H,Webster R G,Webby R J,Ali MA.Continuing threat of influenza (H5N1) virus circulation in Egypt[J].Emerg Infect Dis,2011,17(12):2306-2308.
• [39]Fadel H M,Afifi R.Investigation of avian influenza infection in wild birds in Ismailia and Damietta cities,Egypt[J].Vet World,2017,10(6):695-701.
• [40]Yao Y,Fu S,He B,Chen X,Shao Z,Yang W,Chen J.Complete genome sequences of an H5N1 highly pathogenic avian influenza virus isolated from pigeon in China in 2012[J/OL].Genome Announc,2015,3(6):e01330-15.
• [41]Hassan M M,Hoque M A,Ujvari B,Klaassen M.Live bird markets in Bangladesh as a potentially important source for Avian Influenza Virus transmission[J].Prev Vet Med,2018,156:22-27.
• [42]Zhang Q,Shi J,Deng G,Guo J,Zeng X,He X,Kong H,Gu C,Li X,Liu J,Wang G,Chen Y,Liu L,Liang L,Li Y,Fan J,Wang J,Li W,Guan L,Li Q,Yang H,Chen P,Jiang L,Guan Y,Xin X,Jiang Y,Tian G,Wang X,Qiao C,Li C,Bu Z,Chen H.H7N9influenza viruses are transmissible in ferrets by respiratory droplet[J].Science,2013,341(6144):410-414.
• [43]Teske L,Ryll M,Rautenschlein S.Epidemiological investigations on the role of clinically healthy racing pigeons as a reservoir for avian paramyxovirus-1 and avian influenza virus[J].Avian Pathol,2013,42(6):557-565.
• [44]Mansour S M G,Mohamed F F,Eid A A M,Mor SK,Goyal S M.Co-circulation of paramyxo-and influenza viruses in pigeons in Egypt[J].Avian Pathol,2017,46(4):367-375.
• [45]Li J,Gu M,Liu D,Liu B,Jiang K,Zhong L,Liu K,Sun W,Hu J,Wang X,Hu S,Liu X,Liu X.Phylogenetic and biological characterization of three K1203(H5N8)-like avian influenza A virus reassortants in China in 2014[J].Arch Virol,2016,161(2):289-302.
• [46]Liu K,Gu M,Hu S,Gao R,Li J,Shi L,Sun W,Liu D,Gao Z,Xu X,Hu J,Wang X,Liu X,Chen S,Peng D,Jiao X,Liu X.Genetic and biological characterization of three poultry-origin H5N6 avian influenza viruses with all internal genes from genotype SH9N2 viruses[J].Arch Virol,2018,163(4):947-960.
• [47]Liu K,Gao R,Gu M,Li J,Shi L,Sun W,Liu D,Gao Z,Wang X,Hu J,Liu X,Hu S,Chen S,Gao S,Peng D,Jiao X A,Liu X.Genetic and biological characterization of two reassortant H5N2 avian influenza A viruses isolated from waterfowl in China in 2016[J].Vet Microbiol,2018,224:8-16.
• [48]Liu Y,Han C,Wang X,Lin J,Ma M,Shu Y,Zhou J,Yang H,Liang Q,Guo C,Zhu J,Wei H,Zhao J,Ma Z,Pan J.Influenza A virus receptors in the respiratory and intestinal tracts of pigeons[J].Avian Pathol,2009,38(4):263-266.
• [49]Gao R,Cao B,Hu Y,Feng Z,Wang D,Hu W,Chen J,Jie Z,Qiu H,Xu K,Xu X,Lu H,Zhu W,Gao Z,Xiang N,Shen Y,He Z,Gu Y,Zhang Z,Yang Y,Zhao X,Zhou L,Li X,Zou S,Zhang Y,Li X,Yang L,Guo J,Dong J,Li Q,Dong L,Zhu Y,Bai T,Wang S,Hao P,Yang W,Zhang Y,Han J,Yu H,Li D,Gao G F,Wu G,Wang Y,Yuan Z,Shu Y.Human infection with a novel avian-origin influenza A(H7N9)virus[J].N Engl J Med,2013,368(20):1888-1897.
• [50]Shi J,Deng G,Kong H,Gu C,Ma S,Yin X,Zeng X,Cui P,Chen Y,Yang H,Wan X,Wang X,Liu L,Chen P,Jiang Y,Liu J,Guan Y,Suzuki Y,Li M,Qu Z,Guan L,Zang J,Gu W,Han S,Song Y,Hu Y,Wang Z,Gu L,Yang W,Liang L,Bao H,Tian G,Li Y,Qiao C,Jiang L,Li C,Bu Z,Chen H.H7N9virulent mutants detected in chickens in China pose an increased threat to humans[J].Cell Res,2017,27(12):1409-1421.
• [51]Li C,Chen H.H7N9 influenza virus in China[J].Cold Spring Harb Perspect Med,2020.
• [52]WHO.Influenza at the human-animal interface[EB/OL].https：//www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_28_02_2020.pdf?ua=1.2020.
• [53]Liu Y,Yang Z,Wang X,Chen J,Yao J,Song Y,Lin J,Han C,Duan H,Zhao J.Pigeons are resistant to experimental infection with H7N9 avian influenza virus[J].Avian Pathol,2015,44(5):342-346.
• [54]Uchida Y,Kanehira K,Takemae N,Hikono H,Saito T.Susceptibility of chickens,quail,and pigeons to an H7N9 human influenza virus and subsequent eggpassaged strains[J].Arch Virol,2017,162(1):103-116.
• [55]Rogers G N,Paulson J C.Receptor determinants of human and animal influenza virus isolates:Differences in receptor specificity of the H3 hemagglutinin based on species of origin[J].Virology,1983,127(2):361-373.
• [56]Gambaryan A,Yamnikova S,Lvov D,Tuzikov A,Chinarev A,Pazynina G,Webster R,Matrosovich M,Bovin N.Receptor specificity of influenza viruses from birds and mammals:new data on involvement of the inner fragments of the carbohydrate chain[J].Virology,2005,334(2):276-283.
• [57]Shinya K,Ebina M,Yamada S,Ono M,Kasai N,Kawaoka Y.Influenza virus receptors in the human airway[J].Nature,2006,440(7083):435-436.
• [58]Ma W,Kahn R E,Richt J A.The pig as a mixing vessel for influenza viruses:Human and veterinary implications[J].J Mol Genet Med,2008,3(1):158-166.
• [59]de Graaf M,Fouchier R A.Role of receptor binding specificity in influenza A virus transmission and pathogenesis[J].EMBO J,2014,33(8):823-841.
• [60]Kawai T,Akira S.The role of pattern-recognition receptors in innate immunity:update on Toll-like receptors[J].Nat Immunol,2010,11(5):373-384.
• [61]Lee M S,Kim Y J.Signaling pathways downstream of pattern-recognition receptors and their cross talk[J].Annu Rev Biochem,2007,76:447-480.
• [62]Meylan E,Tschopp J,Karin M.Intracellular pattern recognition receptors in the host response[J].Nature,2006,442(7098):39-44.
• [63]Takeuchi O,Akira S.Pattern recognition receptors and inflammation[J].Cell,2010,140(6):805-820.
• [64]Kawai T,Akira S.The roles of TLRs,RLRs and NLRs in pathogen recognition[J].Int Immunol,2009,21(4):317-337.
• [65]Kato H,Takahasi K,Fujita T.RIG-I-like receptors:cytoplasmic sensors for non-self RNA[J].Immunol Rev,2011,243(1):91-98.
• [66]Loo Y M,Gale M Jr.Immune signaling by RIG-I-like receptors[J].Immunity,2011,34(5):680-692.
• [67]Kato H,Takeuchi O,Sato S,Yoneyama M,Yamamoto M,Matsui K,Uematsu S,Jung A,Kawai T,Ishii K J,Yamaguchi O,Otsu K,Tsujimura T,Koh C S,Reis e Sousa C,Matsuura Y,Fujita T,Akira S.Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses[J].Nature,2006,441(7089):101-105.
• [68]Alexander D J,Parsons G,Manvell R J.Experimental assessment of the pathogenicity of eight avian influenza a viruses of H5 subtype for chickens,turkeys,ducks and quail[J].Avian Pathol,1986,15(4):647-662.
• [69]Wood G W,Parsons G,Alexander D J.Replication of influenza A viruses of high and low pathogenicity for chickens at different sites in chickens and ducks following intranasal inoculation[J].Avian Pathol,1995,24(3):545-551.
• [70]Hayashi T,Hiromoto Y,Chaichoune K,Patchimasiri T,Chakritbudsabong W,Prayoonwong N,Chaisilp N,Wiriyarat W,Parchariyanon S,Ratanakorn P,Uchida Y,Saito T.Host cytokine responses of pigeons infected with highly pathogenic Thai avian influenza viruses of subtype H5N1 isolated from wild birds[J/OL].PLo SOne,2011,6(8):e23103.
• [71]Perkins L E,Swayne D E.Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus,geese,ducks,and pigeons[J].Avian Dis,2002,46(1):53-63.
• [72]Klopfleisch R,Werner O,Mundt E,Harder T,Teifke J.Neurotropism of highly pathogenic avian influenza virus A/chicken/Indonesia/2003 (H5N1) in experimentally infected pigeons (Columbia livia f.domestica)[J].Vet Pathol,2006,43(4):463-470.
• [73]Liu Y,Zhou J,Yang H,Yao W,Bu W,Yang B,Song W,Meng Y,Lin J,Han C.Susceptibility and transmissibility of pigeons to Asian lineage highly pathogenic avian influenza virus subtype H5N1[J].Avian Pathol,2007,36(6):461-465.
• [74]Yu Z,Song Y,Zhou H,Xu X,Hu Q,Wu H,Zhang A,Zhou Y,Chen J,Dan H,Luo Q,Li X,Chen H,Jin M.Avian influenza(H5N1)virus in waterfowl and chickens,central China[J].Emerg Infect Dis,2007,13(5):772-775.
• [75]Jia B,Shi J,Li Y,Shinya K,Muramoto Y,Zeng X,Tian G,Kawaoka Y,Chen H.Pathogenicity of Chinese H5N1 highly pathogenic avian influenza viruses in pigeons[J].Arch Virol,2008,153(10):1821-1826.
• [76]Brown J D,Stallknecht D E,Berghaus R D,Swayne DE.Infectious and lethal doses of H5N1 highly pathogenic avian influenza virus for house sparrows (Passer domesticus) and rock pigeons (Columbia livia)[J].JVet Diagn Invest,2009,21(4):437-445.
• [77]Yamamoto Y,Nakamura K,Yamada M,Mase M.Limited susceptibility of pigeons experimentally inoculated with H5N1 highly pathogenic avian influenza viruses[J].J Vet Med Sci,2012,74(2):205-208.
• [78]Kwon J H,Noh Y K,Lee D H,Yuk S S,Erdene-Ochir T O,Noh J Y,Hong W T,Jeong J H,Jeong S,Gwon G B,Song C S,Nahm S S.Experimental infection with highly pathogenic H5N8 avian influenza viruses in the Mandarin duck (Aix galericulata) and domestic pigeon(Columba livia domestica)[J].Vet Microbiol,2017,203:95-102.
• [79]Xiang B,Liang J,You R,Han L,Mei K,Chen L,Chen R,Zhang Y,Dai X,Gao P.Pathogenicity and transmissibility of a highly pathogenic avian influenza virus H5N6 isolated from a domestic goose in Southern China[J].Vet Microbiol,2017,212:16-21.
• [80]Bosco-Lauth A M,Marlenee N L,Hartwig A E,Bowen R A,Root J J.Shedding of clade 2.3.4.4 H5N8and H5N2 highly pathogenic avian influenza viruses in peridomestic wild birds in the US[J].Transbound Emerg Dis,2019,66(3):1301-1305.
• [81]Guan Y,Shortridge K,Krauss S,Chin P,Dyrting K,Ellis T,Webster R,Peiris M.H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China[J].J Virol,2000,74(20):9372-9380.
• [82]Uchida Y,Kanehira K,Takemae N,Hikono H,Saito T.Susceptibility of chickens,quail,and pigeons to an H7N9 human influenza virus and subsequent eggpassaged strains[J].Arch Virol,2017,162(1):103-116.