Verhagen Josanne H, Höfle Ursula, van Amerongen Geert, van de Bildt Marco, Majoor Frank, Fouchier Ron A M, Kuiken Thijs
Department of Viroscience, Erasmus MC, Rotterdam, the Netherlands.
SaBio Group, Instituto de Investigación en Recursos Cinegéticos (IREC)-CSIC-UCLM-JCCM, Cuidad Real, Spain.
J Virol. 2015 Nov;89(22):11507-22. doi: 10.1128/JVI.01765-15. Epub 2015 Sep 2.
Infections of domestic and wild birds with low-pathogenic avian influenza viruses (LPAIVs) have been associated with protective immunity to subsequent infection. However, the degree and duration of immunity in wild birds from previous LPAIV infection, by the same or a different subtype, are poorly understood. Therefore, we inoculated H13N2 (A/black-headed gull/Netherlands/7/2009) and H16N3 (A/black-headed gull/Netherlands/26/2009) LPAIVs into black-headed gulls (Chroicocephalus ridibundus), their natural host species, and measured the long-term immune response and protection against one or two reinfections over a period of >1 year. This is the typical interval between LPAIV epizootics in wild birds. Reinfection with the same virus resulted in progressively less virus excretion, with complete abrogation of virus excretion after two infections for H13 but not H16. However, reinfection with the other virus affected neither the level nor duration of virus excretion. Virus excretion by immunologically naive birds did not differ in total levels of excreted H13 or H16 virus between first- and second-year birds, but the duration of H13 excretion was shorter for second-year birds. Furthermore, serum antibody levels did not correlate with protection against LPAIV infection. LPAIV-infected gulls showed no clinical signs of disease. These results imply that the epidemiological cycles of H13 and H16 in black-headed gulls are relatively independent from each other and depend mainly on infection of first-year birds.
Low-pathogenic avian influenza viruses (LPAIVs) circulate mainly in wild water birds but are occasionally transmitted to other species, including humans, where they cause subclinical to fatal disease. To date, the effect of LPAIV-specific immunity on the epidemiology of LPAIV in wild birds is poorly understood. In this study, we investigated the effect of H13 and H16 LPAIV infection in black-headed gulls on susceptibility and virus excretion of subsequent infection with the same or the other virus within the same breeding season and between breeding seasons. These are the only two LPAIV hemagglutinin subtypes predominating in this species. The findings suggest that H13 and H16 LPAIV cycles in black-headed gull populations are independent of each other, indicate the importance of first-year birds in LPAIV epidemiology, and emphasize the need for alternatives to avian influenza virus (AIV)-specific serum antibodies as evidence of past LPAIV infection and correlates of protection against LPAIV infection in wild birds.
低致病性禽流感病毒（LPAIV）感染家鸟和野鸟与对后续感染的保护性免疫有关。然而，对于先前感染LPAIV（同一亚型或不同亚型）的野鸟的免疫程度和持续时间，人们了解甚少。因此，我们将H13N2（A/黑头鸥/荷兰/7/2009）和H16N3（A/黑头鸥/荷兰/26/2009）LPAIV接种到黑头鸥（Chroicocephalus ridibundus），即它们的自然宿主物种体内，并在超过1年的时间里测量长期免疫反应以及针对一次或两次再感染的保护作用。这是野鸟中LPAIV epizootics之间的典型间隔时间。用同一病毒再感染导致病毒排泄量逐渐减少，H13在两次感染后病毒排泄完全消失，但H16没有。然而，用另一种病毒再感染既不影响病毒排泄水平也不影响其持续时间。免疫未接触过病毒的鸟类在第一年和第二年鸟类中排泄的H13或H16病毒总量没有差异，但第二年鸟类的H13排泄持续时间较短。此外，血清抗体水平与针对LPAIV感染的保护作用不相关。感染LPAIV的鸥没有疾病的临床症状。这些结果表明，黑头鸥中H13和H16的流行病学循环相对彼此独立，并且主要取决于第一年鸟类的感染情况。
低致病性禽流感病毒（LPAIV）主要在野生水鸟中传播，但偶尔会传播给包括人类在内的其他物种，在这些物种中会引起从亚临床到致命的疾病。迄今为止，LPAIV特异性免疫对野生鸟类中LPAIV流行病学的影响了解甚少。在本研究中，我们调查了黑头鸥感染H13和H16 LPAIV对同一繁殖季节内以及不同繁殖季节用同一病毒或另一种病毒进行后续感染的易感性和病毒排泄的影响。这是在该物种中占主导地位的仅有的两种LPAIV血凝素亚型。研究结果表明，黑头鸥种群中H13和H16 LPAIV循环彼此独立，表明第一年鸟类在LPAIV流行病学中的重要性，并强调需要替代禽流感病毒（AIV）特异性血清抗体作为过去LPAIV感染的证据以及野生鸟类针对LPAIV感染的保护相关性。
