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Sathit Pichyangkul Somporn Krasaesub Anan Jongkaewwattana Arunee Thitithanyanont Suwimon Wiboon-ut Kosol Yongvanitchit Amporn Limsalakpetch Utaiwan Kum-Arb Duangrat Mongkolsirichaikul Nuanpan Khemnu Rangsini Mahanonda Jean-Michel Garcia Carl J. Mason Douglas S. Walsh David L. Saunders 《The American journal of tropical medicine and hygiene》2014,90(1):149-152
We studied cross-reactive antibodies against avian influenza H5N1 and 2009 pandemic (p) H1N1 in 200 serum samples from US military personnel collected before the H1N1 pandemic. Assays used to measure antibodies against viral proteins involved in protection included a hemagglutination inhibition (HI) assay and a neuraminidase inhibition (NI) assay. Viral neutralization by antibodies against avian influenza H5N1 and 2009 pH1N1 was assessed by influenza (H5) pseudotyped lentiviral particle-based and H1N1 microneutralization assays. Some US military personnel had cross-neutralizing antibodies against H5N1 (14%) and 2009 pH1N1 (16.5%). The odds of having cross-neutralizing antibodies against 2009 pH1N1 were 4.4 times higher in subjects receiving more than five inactivated whole influenza virus vaccinations than those subjects with no record of vaccination. Although unclear if the result of prior vaccination or disease exposure, these pre-existing antibodies may prevent or reduce disease severity.Outbreaks of 1997 avian influenza H5N1 and 2009 pandemic (p) H1N1 in humans have provided an opportunity to gain insight into cross-reactive immunity. The US military periodically collects and stores serum samples from service members linked to medical records.1 We measured cross-reactive antibodies in stored serum to avian influenza H5N1 and 2009 pH1N1 from US military personnel and identified factors associated with presence of neutralizing antibodies.Two hundred archived serum samples were obtained from the US Department of Defense Serum Repository. They were representative of a wide cross-section of active military personnel at the times of collection, whereas specific geographic information was not available on the individual selected; the cohort represents the general US military population, which is deployed throughout the United States and globally. Fifty samples each were selected from four birth cohorts: (1) < 1949, (2) 1960–1965, (3) 1966–1971, and (4) 1972–1977. Within each cohort, 25 samples were collected in the year 2000 (before the introduction of intranasal live attenuated influenza vaccine [LAIV]), and 25 samples were collected in 2008 (where 51% of donors had received LAIV). It has been suggested that LAIV elicits cross-reactive immunity.2,3 The samples were all collected before the outbreak of 2009 pH1N1, and there have not been any reported outbreaks of H5N1 in US military personnel.Assays used to measure antibodies included a hemagglutination inhibition (HI) assay and a neuraminidase inhibition (NI) assay.4 Viral neutralization by antibodies against H5N1 and 2009 pH1N1 was assessed by influenza (H5) pseudotyped lentiviral particle-based (H5pp)5 and microneutralization assays, respectively. Electronic medical and vaccination records from the Defense Medical Surveillance System (DMSS), which captured records before the serum sample date, were linked to samples and compared with the in vitro results.1The odds ratios (ORs) and 95% confidence intervals (95% CIs) of univariate and multivariate binary logistic regression analyses were used to determine the association between donor characteristics and positive antibody responses. A multiple logistic regression model was constructed, and it included independent variables with a P value of < 0.05 in univariate logistic regression. A P value of < 0.05 was considered to indicate statistical significance. SPSS 12.0 for Windows (SPSS Inc., Chicago, IL) was used to perform all statistical analysis.Cross-reactivity is summarized in 5 and 22.5% for the NI assay. H5pp and NI antibody titers to H5N1 were evenly distributed among birth cohorts and did not differ substantially based on history of vaccination or prior respiratory infections. Of those individuals with neutralizing antibodies to H5N1 (N = 28), 32.1% also had neutralizing antibodies to pH1N1, whereas 19.3% of those individuals with any H5N1-specific antibody response also had neutralizing antibodies to pH1N1 (Characteristics (n) H5N1 2009 pH1N1§ HI assay* % positive (GM titer) H5pp† % positive (GM titer) NI assay‡ % positive (GM titer) HI assay % positive (GM titer) Neutralization % positive (GM titer) NI assay % positive (GM titer) Total 200 0.5 (5.1) 14.0 (21.4) 22.5 (121.6) 5.5 (7.1) 16.5 (20.4) 9.0 (92.8) Birth cohort 1936–1949 (50) 2.0 (5.3) 18.0 (22.0) 24.0 (126.0) 6.0 (7.3) 16.0 (19.5) 12.0 (97.6) 1960–1965 (50) 0.0 (5.0) 16.0 (20.3) 26.0 (129.6) 6.0 (7.7) 30.0 (27.5) 6.0 (90.3) 1966–1971 (50) 0.0 (5.0) 12.0 (23.3) 20.0 (117.9) 10.0 (8.0) 16.0 (23.6) 10.0 (92.2) 1972–1977 (50) 0.0 (5.3) 10.0 (20.0) 20.0 (113.7) 0.0 (5.7) 4.0 (13.6) 8.0 (91.5) Serum collection year Y2000 (100) 0.0 (5.1) 15.0 (21.7) 21.0 (120.3) 7.0 (7.3) 16.0 (20.6) 11.0 (94.5) Y2008 (100) 1.0 (5.2) 13.0 (21.1) 24.0 (123.0) 4.0 (7.0) 17.0 (20.1) 7.0 (91.2) Sex Female (32) 3.1 (5.7) 21.9 (26.3) 12.5 (102.4) 3.1 (6.9) 12.5 (19.2) 6.3 (96.7) Male (168) 0.0 (5.0) 12.5 (20.5) 24.4 (125.7) 6.0 (7.2) 17.3 (20.6) 9.5 (92.1) Any cross-reactive antibody to H5N1 (57) 8.8 (8.9) 19.3 (25.2) 22.8 (119.9) pH1N1 (45) 2.2 (5.3) 28.9 (31.2) 37.8 (165.2) Neutralizing antibodies to H5N1 H5pp (28) 10.7 (9.5) 32.1 (33.6) 25.0 (116.9) 2009 pH1N1 neutralization (33) 3.0 (5.4) 27.3 (28.9) 30.3 (140.3) Lifetime seasonal vaccinations No record (66) 0.0 (5.1) 10.6 (20.2) 27.7 (128.1) 7.6 (7.4) 15.2 (20.6) 12.1 (96.5) 1–5 vaccinations (88) 1.1 (5.2) 15.9 (21.5) 17.0 (109.2) 5.7 (7.1) 17.0 (20.5) 6.8 (89.1) > 5 vaccinations (46) 0.0 (5.1) 15.2 (22.2) 32.6 (138.8) 2.2 (6.8) 17.4 (19.7) 8.7 (95.0) Time since last vaccine No record (66) 0.0 (5.1) 10.6 (20.2) 22.7 (128.1) 7.6 (7.4) 15.2 (20.6) 12.1 (96.5) ≤ 1 year (96) 0.0 (5.1) 15.6 (21.5) 24.0 (120.7) 4.2 (7.1) 19.8 (21.0) 8.3 (91.2) > 1 year (38) 2.6 (5.3) 15.8 (22.4) 18.4 (113.4) 5.2 (6.8) 10.5 (18.3) 5.3 (90.6) Vaccination history lifetime (at least one dose) No record of vaccination (66) 0.0 (5.1) 10.6 (20.2) 22.7 (128.1) 7.6 (7.4) 15.2 (20.6) 12.1 (96.5) Inactivated whole virus (71) 0.0 (5.0) 14.1 (20.4) 22.5 (115.7) 2.8 (6.4) 15.5 (19.6) 5.6 (87.1) Split type (102) 1.0 (5.0) 15.7 (20.4) 21.6 (115.7) 4.9 (6.4) 19.6 (19.6) 6.9 (87.1) Influenza vaccine not otherwise specified (16) 0.0 (5.2) 12.5 (27.9) 37.5 (166.4) 0.0 (6.2) 6.3 (16.1) 12.5 (102.3) Live attenuated intranasal (50) 0.0 (5.1) 10.0 (18.8) 20.0 (112.2) 4.0 (7.0) 18.0 (20.3) 4.0 (85.2) History of respiratory illness No record of illness (119) 0.0 (5.0) 10.1 (18.5) 18.5 (112.6) 4.2 (7.0) 15.1 (20.5) 8.4 (90.7) Influenza-like illness (4) 0.0 (5.0) 25.0 (20.7) 0.0 (80.0) 0.0 (8.4) 25.0 (28.3) 25.0 (100.2) Upper respiratory infection (65) 1.5 (5.4) 23.1 (29.3) 27.7 (135.0) 7.7 (7.3) 18.5 (20.7) 9.2 (93.1) Lower respiratory infection (37) 2.7 (5.6) 18.9 (30.2) 35.1 (157.6) 8.1 (8.1) 21.6 (22.4) 13.5 (108.4) Respiratory illness past year (28) 0 (5.1) 25.0 (25.1) 32.1 (154.9) 7.1 (8.0) 28.6 (24.4) 3.6 (86.3)