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Persistence of maternal antibodies to influenza A virus among captive mallards (Anas platyrhynchos)

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Abstract

Wild waterfowl are maintenance hosts of most influenza A virus (IAV) subtypes and are often the subjects of IAV surveillance and transmission models. While maternal antibodies have been detected in yolks and in nestlings for a variety of wild bird species and pathogens, the persistence of maternal antibodies to IAVs in mallard ducklings (Anas platyrhynchos) has not been previously investigated. Nonetheless, this information is important for a full understanding of IAV transmission dynamics because ducklings protected by maternal antibodies may not be susceptible to infection. In this study, we examined the transfer of IAV-specific maternal antibodies to ducklings. Blood samples were collected approximately every five days from ducklings hatched from hens previously infected with an H6 strain of IAV. Serum samples were tested for antibodies to IAV by an enzyme-linked immunosorbent assay. The median persistence of maternal antibodies in ducklings was 12.5 days (range: 4-33 days) post-hatch. The majority of ducklings (71%) had detectable maternal antibodies from 4 to 17 days post-hatch, while a small subset of individuals (29%) had detectable maternal antibodies for up to 21-33 days post-hatch. Antibody concentrations in hens near the time of egg laying were correlated with maternal antibody concentrations in the initial blood sample collected from ducklings (0-4 days post-hatch). Knowledge of the duration of maternal antibodies in ducklings will aid in the interpretation of IAV serological surveillance results and in the modeling of IAV transmission dynamics in waterfowl.

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Data availability

All data generated or analysed during this study are included in this published article and its supplementary information file (Online Resource 1).

References

  1. Paarlberg PL, Seitzinger AH, Lee JG (2007) Economic impacts of regionalization of a highly pathogenic avian influenza outbreak in the United States. J Agric Appl Econ 39(2):325–333

    Article  Google Scholar 

  2. Brand JM, Verhagen JH, Kroeze EJV, Bildt MW, Bodewes R, Herfst S, Richard M, Lexmond P, Bestebroer TM, Fouchier RA (2018) Wild ducks excrete highly pathogenic avian influenza virus H5N8 (2014-2015) without clinical or pathological evidence of disease. Emerg Microbes Infect 7(1):67. https://doi.org/10.1038/s41426-018-0070-9

    Article  PubMed  PubMed Central  Google Scholar 

  3. Duan L, Bahl J, Smith G, Wang J, Vijaykrishna D, Zhang L, Zhang J, Li K, Fan X, Cheung C (2008) The development and genetic diversity of H5N1 influenza virus in China, 1996-2006. Virol 380(2):243–254

    Article  CAS  Google Scholar 

  4. Gilbert M, Koel BF, Bestebroer TM, Lewis NS, Smith DJ, Fouchier RA (2014) Serological evidence for non-lethal exposures of Mongolian wild birds to highly pathogenic avian influenza H5N1 virus. PLoS ONE 9(12):e113569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Seekings A, Slomka M, Russell C, Howard W, Choudhury B, Nuñéz A, Löndt B, Cox W, Ceeraz V, Thorén P (2018) Direct evidence of H7N7 avian influenza virus mutation from low to high virulence on a single poultry premises during an outbreak in free range chickens in the UK, 2008. Infect Genet Evol 64:13–31

    Article  CAS  PubMed  Google Scholar 

  6. Dietze K, Graaf A, Homeier-Bachmann T, Grund C, Forth L, Pohlmann A, Jeske C, Wintermann M, Beer M, Conraths FJ (2018) From low to high pathogenicity-characterization of H7N7 avian influenza viruses in two epidemiologically linked outbreaks. Transbound Emerg Dis. https://doi.org/10.1111/tbed.12906

    Article  PubMed  Google Scholar 

  7. Hinshaw V, Webster R, Turner B (1980) The perpetuation of orthomyxoviruses and paramyxoviruses in Canadian waterfowl. Can J Microbiol 26(5):622–629

    Article  CAS  PubMed  Google Scholar 

  8. Deliberto TJ, Swafford SR, Nolte DL, Pedersen K, Lutman MW, Schmit BB, Baroch JA, Kohler DJ, Franklin A (2009) Surveillance for highly pathogenic avian influenza in wild birds in the USA. Integr Zool 4(4):426–439

    Article  PubMed  Google Scholar 

  9. Stallknecht DE, Brown JD, Swayne D (2008) Ecology of avian influenza in wild birds. Avian Influenza 1:43–58

    Article  Google Scholar 

  10. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56(1):152–179

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus AD, Fouchier RA (2006) Global patterns of influenza A virus in wild birds. Science 312(5772):384–388

    Article  CAS  PubMed  Google Scholar 

  12. Spackman E, Stallknecht DE, Slemons RD, Winker K, Suarez DL, Scott M, Swayne DE (2005) Phylogenetic analyses of type A influenza genes in natural reservoir species in North America reveals genetic variation. Virus Res 114:89–100

    Article  CAS  PubMed  Google Scholar 

  13. Chin P, Hoffmann E, Webby R, Webster R, Guan Y, Peiris M, Shortridge K (2002) Molecular evolution of H6 influenza viruses from poultry in southeastern China: prevalence of H6N1 influenza viruses possessing seven A/Hong Kong/156/97 (H5N1)-like genes in poultry. J Virol 76(2):507–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Woolcock P, Suarez D, Kuney D (2003) Low-pathogenicity avian influenza virus (H6N2) in chickens in California, 2000-02. Avian Dis 47:872–881

    Article  CAS  PubMed  Google Scholar 

  15. Ip HS, Flint PL, Franson JC, Dusek RJ, Derksen DV, Gill RE, Ely CR, Pearce JM, Lanctot RB, Matsuoka SM (2008) Prevalence of influenza A viruses in wild migratory birds in Alaska: patterns of variation in detection at a crossroads of intercontinental flyways. Virol J 5(1):71

    Article  CAS  Google Scholar 

  16. Reperant L, Rimmelzwaan G, Kuiken T (2009) Avian influenza viruses in mammals. Rev Sci Tech 28(1):137

    Article  CAS  PubMed  Google Scholar 

  17. Vandalen KK, Shriner SA, Sullivan HJ, Root JJ, Franklin AB (2009) Monitoring exposure to avian influenza viruses in wild mammals. Mamm Rev 39(3):167–177

    Article  Google Scholar 

  18. Hasselquist D, Nilsson J-Å (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Phil Trans R Soc Lond B Biol Sci 364(1513):51–60

    Article  Google Scholar 

  19. Grindstaff JL (2008) Maternal antibodies reduce costs of an immune response during development. J Exp Biol 211(5):654–660

    Article  CAS  PubMed  Google Scholar 

  20. Heeb P, Werner I, Kölliker M, Richner H (1998) Benefits of induced host responses against an ectoparasite. Proc R Soc Lond B Biol Sci 265(1390):51–56

    Article  Google Scholar 

  21. Buechler K, Fitze P, Gottstein B, Jacot A, Richner H (2002) Parasite-induced maternal response in a natural bird population. J Anim Ecol 71(2):247–252

    Article  Google Scholar 

  22. Gustafsson E, Mattsson A, Holmdahl R, Mattsson R (1994) Pregnancy in B-cell-deficient mice: postpartum transfer of immunoglobulins prevents neonatal runting and death. Biol Reprod 51(6):1173–1180

    Article  CAS  PubMed  Google Scholar 

  23. Boulinier T, Staszewski V (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23(5):282–288

    Article  PubMed  Google Scholar 

  24. van Dijk JG, Mateman AC, Klaassen M (2014) Transfer of maternal antibodies against avian influenza virus in mallards (Anas platyrhynchos). PLoS ONE 9(11):e112595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Fahey K, Crooks J, Fraser R (1987) Assessment by ELISA of passively acquired protection against infectious bursal disease virus in chickens. Aust Vet J 64(7):203–207

    Article  CAS  PubMed  Google Scholar 

  26. Darbyshire J, Peters R (1985) Humoral antibody response and assessment of protection following primary vaccination of chicks with maternally derived antibody against avian infectious bronchitis virus. Res Vet Sci 38(1):14–21

    Article  CAS  PubMed  Google Scholar 

  27. Hamal KR, Burgess SC, Pevzner I, Erf G (2006) Maternal antibody transfer from dams to their egg yolks, egg whites, and chicks in meat lines of chickens. Poult Sci 85(8):1364–1372

    Article  CAS  PubMed  Google Scholar 

  28. Mesonero A, Suarez DL, Van Santen E, Tang DC, Toro H (2011) Avian influenza in ovo vaccination with replication defective recombinant adenovirus in chickens: vaccine potency, antibody persistence, and maternal antibody transfer. Avian Dis 55(2):285–292

    Article  PubMed  Google Scholar 

  29. Hammouda A, Pearce-Duvet J, Chokri MA, Arnal A, Gauthier-Clerc M, Boulinier T, Selmi S (2011) Prevalence of influenza A antibodies in yellow-legged gull (Larus michahellis) eggs and adults in southern Tunisia. Vector-Borne Zoonotic Dis 11(12):1583–1590

    Article  PubMed  Google Scholar 

  30. Balish AL, Katz JM, Klimov AI (2013) Influenza: propagation, quantification, and storage. Curr Protoc Microbiol 29(1): 15G.1.1–15G.1.24

  31. Reed LJ, Muench H (1938) A simple method of estimating fifty percent endpoints. Am J Epidemiol 27(3):493–497

    Article  Google Scholar 

  32. VanDalen KK, Franklin AB, Mooers NL, Sullivan HJ, Shriner SA (2010) Shedding light on avian influenza H4N6 infection in mallards: modes of transmission and implications for surveillance. PLoS ONE 5(9):e12851

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Shriner SA, VanDalen KK, Root JJ, Sullivan HJ (2016) Evaluation and optimization of a commercial blocking ELISA for detecting antibodies to influenza A virus for research and surveillance of mallards. J Virol Methods 228:130–134

    Article  CAS  PubMed  Google Scholar 

  34. Brown JD, Stallknecht DE, Berghaus RD, Luttrell MP, Velek K, Kistler W, Costa T, Yabsley MJ, Swayne D (2009) Evaluation of a commercial blocking enzyme-linked immunosorbent assay to detect avian influenza virus antibodies in multiple experimentally infected avian species. Clin Vaccine Immunol 16(6):824–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. R Development Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org

  36. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  37. Grindstaff JL, Demas GE, Ketterson ED (2005) Diet quality affects egg size and number but does not reduce maternal antibody transmission in Japanese quail Coturnix japonica. J Anim Ecol 74(6):1051–1058

    Article  Google Scholar 

  38. Faulkner OB, Estevez C, Yu Q, Suarez DL (2013) Passive antibody transfer in chickens to model maternal antibody after avian influenza vaccination. Vet Immunol Immunopathol 152:341–347

    Article  CAS  PubMed  Google Scholar 

  39. Hammouda A, Selmi S, Pearce-Duvet J, Chokri MA, Arnal A, Gauthier-Clerc M, Boulinier T (2012) Maternal antibody transmission in relation to mother fluctuating asymmetry in a long-lived colonial seabird: the yellow-legged gull Larus michahellis. PLoS ONE 7(5):e34966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Velarde R, Calvin SE, Ojkic D, Barker IK, Nagy É (2010) Avian influenza virus H13 circulating in ring-billed gulls (Larus delawarensis) in southern Ontario, Canada. Avian Dis 54:411–419

    Article  PubMed  Google Scholar 

  41. Geffen E, Yom-Tov Y (2001) Factors affecting the rates of intraspecific nest parasitism among Anseriformes and Galliformes. Anim Behav 62(6):1027–1038

    Article  Google Scholar 

  42. Grindstaff JL (2010) Initial levels of maternally derived antibodies predict persistence time in offspring circulation. J Ornithol 151(2):423–428

    Article  Google Scholar 

  43. Patterson R, Youngner J, Weigle W, Dixon F (1962) The metabolism of serum proteins in the hen and chick and secretion of serum proteins by the ovary of the hen. J Gen Phys 45(3):501–513

    Article  CAS  Google Scholar 

  44. Kaleta E, Siegmann O, Lai K, Aussum D (1977) Kinetics of NDV-specific antibodies in chickens. VI. Elimination of Maternal and Injected Antibodies. Berl Munch Tierarztl Wochenschr 90:131–134

    CAS  PubMed  Google Scholar 

  45. Pearce-Duvet JM, Gauthier-Clerc M, Jourdain E, Boulinier T (2009) Maternal antibody transfer in yellow-legged gulls. Emerg Infect Dis 15(7):1147

    Article  PubMed  PubMed Central  Google Scholar 

  46. Chen X, Qi Y, Wang H, Wang Y, Wang H, Ni H (2018) Prevalence of multiple subtypes of avian influenza virus antibodies in egg yolks of mallard (Anas platyrhynchos) and white-winged terns (Chlidonias leucopterus) in the northeastern Republic of China. J Wildl Dis. https://doi.org/10.7589/2017-10-253

    Article  PubMed  Google Scholar 

  47. Pepin KM, Kay SL, Golas BD, Shriner SS, Gilbert AT, Miller RS, Graham AL, Riley S, Cross PC, Samuel MD (2017) Inferring infection hazard in wildlife populations by linking data across individual and population scales. Ecol Lett 20(3):275–292

    Article  PubMed  Google Scholar 

  48. Munster VJ, Baas C, Lexmond P, Waldenström J, Wallensten A, Fransson T, Rimmelzwaan GF, Beyer WE, Schutten M, Olsen B (2007) Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog 3(5):e61. https://doi.org/10.1371/journal.ppat.0030061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Segovia KM, Stallknecht DE, Kapczynski DR, Stabler L, Berghaus RD, Fotjik A, Latorre-Margalef N, França MS (2017) Adaptive heterosubtypic immunity to low pathogenic avian influenza viruses in experimentally infected mallards. PLoS ONE 12(1):e0170335. https://doi.org/10.1371/journal.pone.0170335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the National Wildlife Research Center Animal Care staff for animal husbandry and veterinary care, and Kaci VanDalen, Jeremy Ellis, Nick Dannemiller, and Molly Selleck for assistance in data collection. In addition, we thank Kaci VanDalen for manuscript review, and Enrique Doster for assistance with data analysis. The USDA endorses no commercial products used in this study.

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Correspondence to Katherine L. Dirsmith.

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Welfare of animals

All applicable national and institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted. The study was conducted under NWRC IACUC Approval QA-1912.

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

This study was funded by the United States Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services.

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Handling Editor: Ayato Takada.

Electronic supplementary material

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Online resource 1

Hen and duckling influenza A virus antibody concentrations. Hen sera were collected monthly and duckling sera were collected approximately every five days. Hen IAV antibody concentrations near the time of laying and duckling IAV antibody concentrations were determined by ELISA and are represented here as S/N ratios. Each duckling’s S/N ratio is listed in association with its corresponding band number, nest and clutch identification, hatch date, corresponding hen band number, and corresponding hen S/N ratio. (CSV 40 kb)

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Dirsmith, K.L., Jeffrey Root, J., Bentler, K.T. et al. Persistence of maternal antibodies to influenza A virus among captive mallards (Anas platyrhynchos). Arch Virol 163, 3235–3242 (2018). https://doi.org/10.1007/s00705-018-3978-4

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