Publications by authors named "Tran Nhu Duong"

43 Publications

Novel Mutation of SARS-CoV-2, Vietnam, July 2020.

Emerg Infect Dis 2021 May 1;27(5):1519-1521. Epub 2021 Mar 1.

A cluster of severe acute respiratory syndrome coronavirus 2 infections in Danang, Vietnam, began July 25, 2020, and resulted in 551 confirmed cases and 35 deaths as of February 2021. We analyzed 26 sequences from this cluster and identified a novel shared mutation in nonstructural protein 9, suggesting a single introduction into Vietnam.
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http://dx.doi.org/10.3201/eid2705.210013DOI Listing
May 2021

Coxsackieviruses A6 and A16 associated with hand, foot, and mouth disease in Vietnam, 2008-2017: Essential information for rational vaccine design.

Vaccine 2020 12 19;38(52):8273-8285. Epub 2020 Nov 19.

Department of Virology II, National Institute of Infectious Diseases, Tokyo, Japan.

Development of multivalent hand, foot, and mouth disease (HFMD) vaccines against enterovirus A71 (EV-A71) and several non-EV-A71 enteroviruses is needed for this life-threatening disease with a huge economic burden in Asia-Pacific countries. Comprehensive studies on the molecular epidemiology and genetic and antigenic characterization of major causative enteroviruses will provide information for rational vaccine design. Compared with molecular studies on EV-A71, that for non-EV-A71 enteroviruses remain few and limited in Vietnam. Therefore, we conducted a 10-year study on the circulation and genetic characterization of coxsackievirus A16 (CV-A16) and CV-A6 isolated from patients with HFMD in Northern Vietnam between 2008 and 2017. Enteroviruses were detected in 2228 of 3212 enrolled patients. Of the 42 serotypes assigned, 28.4% and 22.4% accounted for CV-A6 and CV-A16, being the second and the third dominant serotypes after EV-A71 (31.7%), respectively. The circulation of CV-A16 and CV-A6 showed a wide geographic distribution and distinct periodicity. Phylogenetic analyses revealed that the majority of Vietnamese CV-A6 and CV-A16 strains were located within the largest sub-genotypes or sub-genogroups. These comprised strains isolated from patients with HFMD worldwide during the past decade and the Vietnamese strains have been evolving in a manner similar to the strains circulating worldwide. Amino acid sequences of the putative functional loops on VP1 and other VPs among Vietnamese CV-A6 and CV-A16 isolates were highly conserved. Moreover, the functional loop patterns of VP1 were similar to the dominant patterns found worldwide, except for the T164K substitution on the EF loop in Vietnamese CV-A16. The findings suggest that the development of a universal HFMD vaccine, at least in Vietnam, must target CV-A6 and CV-A16 as two of the three major HFMD-causing serotypes. Vietnamese isolates or their genome sequences can be considered for rational vaccine design.
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http://dx.doi.org/10.1016/j.vaccine.2020.11.031DOI Listing
December 2020

Transmission of SARS-CoV 2 During Long-Haul Flight.

Emerg Infect Dis 2020 Nov 18;26(11):2617-2624. Epub 2020 Sep 18.

To assess the role of in-flight transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), we investigated a cluster of cases among passengers on a 10-hour commercial flight. Affected persons were passengers, crew, and their close contacts. We traced 217 passengers and crew to their final destinations and interviewed, tested, and quarantined them. Among the 16 persons in whom SARS-CoV-2 infection was detected, 12 (75%) were passengers seated in business class along with the only symptomatic person (attack rate 62%). Seating proximity was strongly associated with increased infection risk (risk ratio 7.3, 95% CI 1.2-46.2). We found no strong evidence supporting alternative transmission scenarios. In-flight transmission that probably originated from 1 symptomatic passenger caused a large cluster of cases during a long flight. Guidelines for preventing SARS-CoV-2 infection among air passengers should consider individual passengers' risk for infection, the number of passengers traveling, and flight duration.
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http://dx.doi.org/10.3201/eid2611.203299DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7588538PMC
November 2020

The First 100 Days of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Control in Vietnam.

Clin Infect Dis 2021 05;72(9):e334-e342

Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom.

Background: One hundred days after severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) was first reported in Vietnam on 23 January, 270 cases were confirmed, with no deaths. We describe the control measures used by the government and their relationship with imported and domestically acquired case numbers, with the aim of identifying the measures associated with successful SARS-CoV-2 control.

Methods: Clinical and demographic data on the first 270 SARS-CoV-2 infected cases and the timing and nature of government control measures, including numbers of tests and quarantined individuals, were analyzed. Apple and Google mobility data provided proxies for population movement. Serial intervals were calculated from 33 infector-infectee pairs and used to estimate the proportion of presymptomatic transmission events and time-varying reproduction numbers.

Results: A national lockdown was implemented between 1 and 22 April. Around 200 000 people were quarantined and 266 122 reverse transcription polymerase chain reaction (RT-PCR) tests conducted. Population mobility decreased progressively before lockdown. In total, 60% (163/270) of cases were imported; 43% (89/208) of resolved infections remained asymptomatic for the duration of infection. The serial interval was 3.24 days, and 27.5% (95% confidence interval [CI], 15.7%-40.0%) of transmissions occurred presymptomatically. Limited transmission amounted to a maximum reproduction number of 1.15 (95% CI, .·37-2.·36). No community transmission has been detected since 15 April.

Conclusions: Vietnam has controlled SARS-CoV-2 spread through the early introduction of mass communication, meticulous contact tracing with strict quarantine, and international travel restrictions. The value of these interventions is supported by the high proportion of asymptomatic and imported cases, and evidence for substantial presymptomatic transmission.
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http://dx.doi.org/10.1093/cid/ciaa1130DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7454342PMC
May 2021

Influenza A(H1N1)pdm09 but not A(H3N2) virus infection induces durable sero-protection: results from the Ha Nam Cohort.

J Infect Dis 2020 Jun 2. Epub 2020 Jun 2.

Oxford University Clinical Research Unit and Wellcome Trust Major Overseas Programme, Hanoi, Viet Nam.

Background: The extent to which influenza recurrence depends upon waning immunity from prior-infection is undefined. We used antibody titres of Ha-Nam cohort participants to estimate protection curves and decay trajectories.

Methods: 270 households participated in influenza-like-illness surveillance and provided blood at intervals spanning RTPCR-confirmed transmission. Sera were tested in haemagglutination inhibition assay. Infection was defined as RTPCR+ influenza-like-illness and/or seroconversion. Median protective titres were estimated using scaled-logistic-regression to model pre-transmission titre against infection status in that season, limiting analysis to households with infection(s). Titres were modelled against month since infection using mixed-effects linear regression to estimate decay and when titres fell below protection-thresholds.

Results: 295 and 314 participants were infected with H1N1pdm09-like and A/Perth/16/09-like (H3N2Pe09) viruses, respectively between December 2008-2012. The proportion of householders not-infected (protected) rose more steeply with titre for H1N1pdm09 than for H3N2Pe09, and estimated 50% protection titres were 19.6 and 37.3, respectively. Post-infection titres started higher against H3N2Pe09 but decayed more steeply than against H1N1pdm09. Sero-protection was estimated to be sustained against H1N1pdm09 but to wane by 8-months for H3N2Pe09.

Conclusions: Estimates indicate that infection induces durable sero-protection against H1N1pdm09 but not H3N2Pe09, which could in part account for the younger age of A(H1N1) versus A(H3N2) cases.
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http://dx.doi.org/10.1093/infdis/jiaa293DOI Listing
June 2020

Severe Acute Respiratory Syndrome Coronavirus 2 Shedding by Travelers, Vietnam, 2020.

Emerg Infect Dis 2020 07 21;26(7):1624-1626. Epub 2020 Jun 21.

We analyzed 2 clusters of 12 patients in Vietnam with severe acute respiratory syndrome coronavirus 2 infection during January-February 2020. Analysis indicated virus transmission from a traveler from China. One asymptomatic patient demonstrated virus shedding, indicating potential virus transmission in the absence of clinical signs and symptoms.
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http://dx.doi.org/10.3201/eid2607.200591DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7323563PMC
July 2020

Epidemiological and comparative genomic analysis of Bacillus anthracis isolated from northern Vietnam.

PLoS One 2020 21;15(2):e0228116. Epub 2020 Feb 21.

Department of Veterinary Science, National Institute of Infectious Diseases, Tokyo, Japan.

To understand the epidemiological and genetic background of anthrax cases occurring in Vietnam from 2011 to 2015, we surveilled and genetically analyzed Bacillus anthracis isolated in the north of the country. Epidemiological surveillance showed that most human cutaneous anthrax cases occurred in association with animal dissection. Whole-genome sequences were obtained from six B. anthracis strains from human patients with cutaneous anthrax in the endemic area. Comparative genomic analysis showed that the genetic homogeneity among Vietnamese B. anthracis strains was very high. All Vietnamese B. anthracis strains belonged to the canSNP lineage of A.Br.011/009, which mostly consists of strains of the trans-Eurasian (TEA) group, including the most closely related strain, Carbosap. To clarify the genetic diversity of Vietnamese strains and strains belonging to A.Br.011/009 and A.Br.008/011 canSNP lineages, we applied a reference genome-based single-nucleotide polymorphism (SNP) and gene-by-gene genomic analysis (whole-genome MLST) strategy. The phylogeny from core genome SNPs revealed that the Vietnamese strains were positioned close to each other; moreover, several SNPs specific to Vietnamese B. anthracis were identified. Whole-genome MLST analysis revealed the differences in the number of SNPs between Vietnamese strains, which could enable discrimination at the strain level.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0228116PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7034820PMC
April 2020

Plans for Nationwide Serosurveillance Network in Vietnam.

Emerg Infect Dis 2020 01;26(1)

In recent years, serosurveillance has gained momentum as a way of determining disease transmission and immunity in populations, particularly with respect to vaccine-preventable diseases. At the end of 2017, the Oxford University Clinical Research Unit and the National Institute of Hygiene and Epidemiology held a meeting in Vietnam with national policy makers, researchers, and international experts to discuss current seroepidemiologic projects in Vietnam and future needs and plans for nationwide serosurveillance. This report summarizes the meeting and the plans that were discussed to set up nationwide serosurveillance in Vietnam.
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http://dx.doi.org/10.3201/eid2601.190641DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6924907PMC
January 2020

A Phase 2/3 double blinded, randomized, placebo-controlled study in healthy adult participants in Vietnam to examine the safety and immunogenicity of an inactivated whole virion, alum adjuvanted, A(H5N1) influenza vaccine (IVACFLU-A/H5N1).

Vaccine 2020 02 4;38(6):1541-1550. Epub 2019 Dec 4.

PATH, Seattle, USA. Electronic address:

Background: A global shortfall of vaccines for avian influenza A(H5N1) would occur, especially in low- and-middle income countries, if a pandemic were to occur. To address this issue, development of a pre-pandemic influenza vaccine was initiated in 2012, leveraging a recently established influenza vaccine manufacturing capacity in Vietnam.

Methods: This was a Phase 2/3, double-blinded, randomized, placebo-controlled study to test the safety and immunogenicity of IVACFLU-A/H5N1 vaccine in healthy adults. Phase 2 was a dose selection study, in which 300 participants were randomized to one of the three groups (15 mcg, 30 mcg, or placebo). Safety and immunogenicity were assessed in all participants. In Phase 3, 630 participants were randomized to receive the IVACFLU-A/H5N1 vaccine dose selected in Phase 2 (15 mcg, n = 525) or placebo (n = 105). Safety was assessed in all Phase 3 participants and immunogenicity was measured in a subset of participants.

Results: The vaccine was well tolerated and most of the adverse events were mild and of short duration. Mild pain at the injection site was the most common adverse event seen in 60 percent of participants in the vaccine group in Phase 3. In Phase 2, both 15 mcg and 30 mcg doses were immunogenic, so the lower dose was selected for further testing in Phase 3. In Phase 3 overall seroconversion rates were 68 percent for hemagglutination inhibition (HI), 51 percent for microneutralization (MN) and 56 percent for single radial hemolysis (SRH). The seroprotection rates were 44 percent for HI, 41 percent for MN and 55 percent for SRH. The GMT ratio was 5.31 and 3.7 for HI and MN respectively; GMA was 4.75 for the SRH.

Conclusion: The IVACFLU A/H5N1 was safe and immunogenic. Development of this pandemic avian influenza vaccine is a welcome addition to the limited global pool of these vaccines. ClinicalTrials.gov register NCT02612909.
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http://dx.doi.org/10.1016/j.vaccine.2019.11.059DOI Listing
February 2020

Sero-Prevalence Surveillance to Predict Vaccine-Preventable Disease Outbreaks; A Lesson from the 2014 Measles Epidemic in Northern Vietnam.

Open Forum Infect Dis 2019 Mar 24;6(3):ofz030. Epub 2019 Jan 24.

Oxford University Clinical Research Unit, Wellcome Trust Asia Programme, Hanoi, Vietnam.

Background: During the first half of 2014, a severe outbreak of measles occurred in northern Vietnam, causing 15 033 confirmed cases and 146 deaths.

Methods: To evaluate the population-level seroprevalence of protection against measles in the period before the outbreak, we made use of an existing age-stratified serum bank, collected over the year before the outbreak, between November 2012 and December 2013, from 4 sites across the country (Hanoi, Hue, Dak Lak, and Ho Chi Minh City). Data from the UNICEF's Multiple Indicator Clustered Surveys (MICS), carried out in Vietnam during the first quarter of 2014, were used to assess the vaccine coverage in 6 ecological regions of Vietnam.

Results: Results revealed a large discrepancy between levels of protection, as estimated from the serology and vaccine coverage estimated by UNICEF's MICS. Variation in seroprevalence across locations and age groups corresponded with reported numbers of measles cases, most of which were among the 0-2-year-old age group and in the northern part of the country.

Conclusions: Our study presents a strong case in favor of a serosurveillance sentinel network that could be used to proactively tune vaccination policies and other public health interventions.
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http://dx.doi.org/10.1093/ofid/ofz030DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6405937PMC
March 2019

Geographical and temporal patterns of rabies post exposure prophylaxis (PEP) incidence in humans in the Mekong River Delta and Southeast Central Coast regions in Vietnam from 2005 to 2015.

PLoS One 2018 10;13(4):e0194943. Epub 2018 Apr 10.

International Livestock Research Institute, Hanoi, Vietnam.

Background: In Vietnam, rabies has been a notifiable disease for more than 40 years. Over the last five years, on average, more than 350,000 people per year have been bitten by dogs and cats while more than 80 human deaths have been reported yearly. No studies have been conducted to evaluate the geographical and temporal patterns of rabies in humans in Vietnam. Therefore, the main objective of this study was to assess the geographical and temporal distributions of rabies post exposure prophylaxis (PEP) incidence in humans in Vietnam from 2005 to 2015.

Methods: Average incidence rabies (AIR) PEP rates for every 3 or 4 years (2005-2008, 2009-2012 and 2013-2015) were calculated to describe the spatial distribution of rabies PEP. Hotspot analysis was implemented to identify patterns of spatial significance using the Getis-Ord Gi statistic. For temporal pattern analysis, two regions [Mekong River Delta (MRD) and Southeast Central Coast (SCC)], with the highest incidence rates, and the seasonal-decomposition procedure based on loess (STL), were compared to assess their temporal patterns of rabies PEP.

Findings: We found hotspots in southern Vietnam and coldspots in northern Vietnam during the study period. Rabies cases were limited to specific areas. In addition, the hotspot analysis showed that new risk areas were identified in each period which were not observed in incidence rate maps. The seasonal plots showed seasonal patterns with a strong peak in February/July and a minor peak in October/December in the MRD region. However, in the SCC, a small peak was detected at the early part of each year and a strong peak in the middle of each year.

Conclusion: Our findings provide insight into understanding the geographical and seasonal patterns of rabies PEP in Vietnam. This study provides evidence to aid policy makers when making decisions and investing resources. Such information may also be utilized to raise public awareness to prevent rabies exposures and reduce unnecessary PEP.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0194943PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5892892PMC
July 2018

Incidence of dengue and chikungunya viruses in mosquitoes and human patients in border provinces of Vietnam.

Parasit Vectors 2017 Nov 9;10(1):556. Epub 2017 Nov 9.

Cirad, Intertryp, UMR 17, TA-A17/G, Campus International de Baillarguet, 34398 Cedex 5, Montpellier, France.

Background: Dengue virus remains a major threat in Vietnam, while chikungunya virus is expected to become one. Surveillance was conducted from 2012 to 2014 in Vietnam to assess the presence of dengue and chikungunya viruses in patients hospitalized with acute fever in five Vietnam provinces neighboring Lao PDR and Cambodia. Surveillance was extended to mosquitoes present in the vicinity of the patients' households.

Results: A total 558 human serum samples were collected along with 1104 adult mosquitoes and 12,041 larvae from 2250 households. Dengue virus was found in 17 (3%) human serum samples and in 9 (0.8%) adult mosquitoes. Chikungunya virus was detected in 2 adult mosquitoes (0.18%) while no chikungunya virus was detected in humans. Differing densities of mosquito populations were found, with the highest in the Long An Province border with Cambodia. Long An Province also displayed the lowest rate of infection, despite a very high Breteau Index, high human population density and presence of the main cross border road system. The highest incidence was found in Dac Nong Province, where the Breteau and Container indices were the second lowest. Dengue virus was detected in five Aedes albopictus, three Aedes aegypti and one Culex vishnui. Chikungunya virus was detected in two Ae. aegypti. All infected mosquitoes belonged to haplotypes described in other parts of the world and a number of novel haplotypes were found among uninfected mosquitoes.

Conclusions: Dengue is considered to be regularly introduced to Vietnam from Cambodia, mostly through human movement. The data reported here provides a complementary picture. Due to intensive international trade, long-distance transportation of mosquito populations may play a role in the regular importation of dengue in Vietnam through Ho Chi Minh City. It is important to decipher the movement of mosquitoes in Vietnam, not only at the Lao PDR and Cambodia borders but also through international trade routes. Mosquito surveillance programs should address and follow mosquito populations instead of mosquito species.
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http://dx.doi.org/10.1186/s13071-017-2422-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5680899PMC
November 2017

Valine/isoleucine variants drive selective pressure in the VP1 sequence of EV-A71 enteroviruses.

BMC Infect Dis 2017 05 8;17(1):333. Epub 2017 May 8.

Cirad, UMR 17, Intertryp, TA-A17/G, Campus International de Baillarguet, 34398, Montpellier Cedex 5, France.

Background: In 2011-2012, Northern Vietnam experienced its first large scale hand foot and mouth disease (HFMD) epidemic. In 2011, a major HFMD epidemic was also reported in South Vietnam with fatal cases. This 2011-2012 outbreak was the first one to occur in North Vietnam providing grounds to study the etiology, origin and dynamic of the disease. We report here the analysis of the VP1 gene of strains isolated throughout North Vietnam during the 2011-2012 outbreak and before.

Methods: The VP1 gene of 106 EV-A71 isolates from North Vietnam and 2 from Central Vietnam were sequenced. Sequence alignments were analyzed at the nucleic acid and protein level. Gene polymorphism was also analyzed. A Factorial Correspondence Analysis was performed to correlate amino acid mutations with clinical parameters.

Results: The sequences were distributed into four phylogenetic clusters. Three clusters corresponded to the subgenogroup C4 and the last one corresponded to the subgenogroup C5. Each cluster displayed different polymorphism characteristics. Proteins were highly conserved but three sites bearing only Isoleucine (I) or Valine (V) were characterized. The isoleucine/valine variability matched the clusters. Spatiotemporal analysis of the I/V variants showed that all variants which emerged in 2011 and then in 2012 were not the same but were all present in the region prior to the 2011-2012 outbreak. Some correlation was found between certain I/V variants and ethnicity and severity.

Conclusions: The 2011-2012 outbreak was not caused by an exogenous strain coming from South Vietnam or elsewhere but by strains already present and circulating at low level in North Vietnam. However, what triggered the outbreak remains unclear. A selective pressure is applied on I/V variants which matches the genetic clusters. I/V variants were shown on other viruses to correlate with pathogenicity. This should be investigated in EV-A71. I/V variants are an easy and efficient way to survey and identify circulating EV-A71 strains.
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http://dx.doi.org/10.1186/s12879-017-2427-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5422960PMC
May 2017

Epidemiology and etiology of influenza-like-illness in households in Vietnam; it's not all about the kids!

J Clin Virol 2016 09 26;82:126-132. Epub 2016 Jul 26.

Oxford University Clinical Research Unit and Wellcome Trust Major Overseas Programme, Vietnam; The University of Melbourne, Peter Doherty Institute for Infection and Immunity, Department of Microbiology and Immunology, Parkville, Victoria, Australia. Electronic address:

Background: Household studies provide opportunities to understand influenza-like-illness (ILI) transmission, but data from (sub)tropical developing countries are scarce.

Objective: To determine the viral etiology and epidemiology of ILI in households.

Study Design: ILI was detected by active case finding amongst a cohort of 263 northern Vietnam households between 2008 and 2013. Health workers collected nose and throat swabs for virus detection by multiplex real-time RT-PCR.

Results: ILI was detected at least once in 219 (23.7%) of 945 household members. 271 (62.3%) of 435 nose/throat swabs were positive for at least one of the 15 viruses tested. Six viruses predominated amongst positive swabs: Rhinovirus (28%), Influenza virus (17%), Coronavirus (8%), Enterovirus (5%), Respiratory syncytial virus (3%), Metapneumovirus virus (2.5%) and Parainfluenza virus 3 (1.8%). There was no clear seasonality, but 78% of episodes occurred in Winter/Spring for Influenza compared to 32% for Rhinovirus. Participants, on average, suffered 0.49 ILI, and 0.29 virus-positive ILI episodes, with no significant effects of gender, age, or household size. In contrast to US and Australian community studies, the frequency of ILI decreased as the number of household members aged below 5 years increased (p=0.006).

Conclusion: The findings indicate the need for tailored ILI control strategies, and for better understanding of how local childcare practices and seasonality may influence transmission and the role of children.
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http://dx.doi.org/10.1016/j.jcv.2016.07.014DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4994428PMC
September 2016

Association between Hemagglutinin Stem-Reactive Antibodies and Influenza A/H1N1 Virus Infection during the 2009 Pandemic.

J Virol 2016 07 24;90(14):6549-6556. Epub 2016 Jun 24.

Oxford University Clinical Research Unit and Wellcome Trust Major Overseas Programme, Hanoi, Vietnam

Unlabelled: The discovery of influenza virus broadly neutralizing (BrN) antibodies prompted efforts to develop universal vaccines. Influenza virus stem-reactive (SR) broadly neutralizing antibodies have been detected by screening antibody phage display libraries. However, studies of SR BrN antibodies in human serum, and their association with natural infection, are limited. To address this, pre- and postpandemic sera from a prospective community cohort study in Vietnam were assessed for antibodies that inhibit SR BrN monoclonal antibody (MAb) (C179) binding to H1N1 pandemic 2009 virus (H1N1pdm09). Of 270 households, 33 with at least one confirmed H1N1pdm09 illness or at least two seroconverters were included. The included households comprised 71 infected and 41 noninfected participants. Sera were tested as 2-fold dilutions between 1:5 and 1:40. Fifty percent C179 inhibition (IC50) titers did not exceed 10, although both IC50 titers and percent C179 inhibition by sera diluted 1:5 or 1:10 correlated with hemagglutination inhibition (HI) and microneutralization (MN) titers (all P < 0.001). Thirteen (12%) participants had detectable prepandemic IC50 titers, but only one reached a titer of 10. This proportion increased to 44% after the pandemic, when 39 participants had a titer of 10, and 67% of infected compared to 44% of noninfected had detectable IC50 titers (P < 0.001). The low levels of SR antibodies in prepandemic sera were not associated with subsequent H1N1pdm09 infection (P = 0.241), and the higher levels induced by H1N1pdm09 infection returned to prepandemic levels within 2 years. The findings indicate that natural infection induces only low titers of SR antibodies that are not sustained.

Importance: Universal influenza vaccines could have substantial health and economic benefits. The focus of universal vaccine research has been to induce antibodies that prevent infection by diverse influenza virus strains. These so-called broadly neutralizing antibodies are readily detected in mice and ferrets after infection with a series of distinct influenza virus strains. The 2009 H1N1 pandemic provided an opportunity to investigate whether infection with a novel strain induced broadly neutralizing antibodies in humans. We found that broadly neutralizing antibodies were induced, but levels were low and poorly maintained. This could represent an obstacle for universal vaccine development and warrants further investigation.
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http://dx.doi.org/10.1128/JVI.00093-16DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4936154PMC
July 2016

Surveillance of dengue and chikungunya infection in Dong Thap, Vietnam: A 13-month study.

Asian Pac J Trop Med 2016 Jan 19;9(1):39-43. Epub 2015 Dec 19.

National Institute of Hygiene and Epidemiology, 1 Yersin Street, 10000 Hanoi, Viet Nam. Electronic address:

Objective: To establish a surveillance in Dong Thap, at the border with Cambodia by assessing the presence of DENV serotypes and CHIKV among patients hospitalized at Dong Thap general hospital.

Methods: Cross-sectional descriptive analysis was conducted on a cohort of 131 patients hospitalized with acute fever and symptoms compatible with dengue or chikungunya. The study was conducted from January 2012 to February 2013. The full clinical picture was established as well as serological and molecular detection. Serological analysis was sequentially performed on blood samples collected on admission and an average of seven days after admission. The detection of IgM antibody to DENV was performed by IgM capture ELISA and the detection of DENV and CHIKV RNA was done by reverse-transcription multiplex PCR.

Results: 101 patients out of 131 (77%) were confirmed with dengue. All four dengue serotypes were detected with a predominance of DENV2 and DENV4. No chikungunya infection was detected although reported in neighboring Cambodia. A differential efficiency of serological dengue detection was observed. Efficiency was 29% upon admission and 53% after seven days on the same patients. 30 patients out of 131 (23%) were negative with both DENV and CHIKV.

Conclusions: Dengue is at risk of being underestimated and chikungunya is not systematically detected. Changes in detection and surveillance procedures are therefore discussed to increase efficiency of dengue detection and continue the monitoring the emergence of CHIKV in Dong Thap province and in Vietnam.
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http://dx.doi.org/10.1016/j.apjtm.2015.12.008DOI Listing
January 2016

Seasonality of absolute humidity explains seasonality of influenza-like illness in Vietnam.

Epidemics 2015 Dec 28;13:65-73. Epub 2015 Aug 28.

Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Hanoi, Viet Nam; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK.

Background: Experimental and ecological studies have shown the role of climatic factors in driving the epidemiology of influenza. In particular, low absolute humidity (AH) has been shown to increase influenza virus transmissibility and has been identified to explain the onset of epidemics in temperate regions. Here, we aim to study the potential climatic drivers of influenza-like illness (ILI) epidemiology in Vietnam, a tropical country characterized by a high diversity of climates. We specifically focus on quantifying and explaining the seasonality of ILI.

Methods: We used 18 years (1993-2010) of monthly ILI notifications aggregated by province (52) and monthly climatic variables (minimum, mean, maximum temperatures, absolute and relative humidities, rainfall and hours of sunshine) from 67 weather stations across Vietnam. Seasonalities were quantified from global wavelet spectra, using the value of the power at the period of 1 year as a measure of the intensity of seasonality. The 7 climatic time series were characterized by 534 summary statistics which were entered into a regression tree to identify factors associated with the seasonality of AH. Results were extrapolated to the global scale using simulated climatic times series from the NCEP/NCAR project.

Results: The intensity of ILI seasonality in Vietnam is best explained by the intensity of AH seasonality. We find that ILI seasonality is weak in provinces experiencing weak seasonal fluctuations in AH (annual power <17.6), whereas ILI seasonality is strongest in provinces with pronounced AH seasonality (power >17.6). In Vietnam, AH and ILI are positively correlated.

Conclusions: Our results identify a role for AH in driving the epidemiology of ILI in a tropical setting. However, in contrast to temperate regions, high rather than low AH is associated with increased ILI activity. Fluctuation in AH may be the climate factor that underlies and unifies the seasonality of ILI in both temperate and tropical regions. Alternatively, the mechanism of action of AH on disease transmission may be different in cold-dry versus hot-humid settings.
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http://dx.doi.org/10.1016/j.epidem.2015.06.002DOI Listing
December 2015

Field evaluation of the establishment potential of wMelPop Wolbachia in Australia and Vietnam for dengue control.

Parasit Vectors 2015 Oct 28;8:563. Epub 2015 Oct 28.

Bio21 Institute and School of BioSciences, University of Melbourne, Parkville, Australia.

Background: Introduced Wolbachia bacteria can influence the susceptibility of Aedes aegypti mosquitoes to arboviral infections as well as having detrimental effects on host fitness. Previous field trials demonstrated that the wMel strain of Wolbachia effectively and durably invades Ae. aegypti populations. Here we report on trials of a second strain, wMelPop-PGYP Wolbachia, in field sites in northern Australia (Machans Beach and Babinda) and central Vietnam (Tri Nguyen, Hon Mieu Island), each with contrasting natural Ae. aegypti densities.

Methods: Mosquitoes were released at the adult or pupal stages for different lengths of time at the sites depending on changes in Wolbachia frequency as assessed through PCR assays of material collected through Biogents-Sentinel (BG-S) traps and ovitraps. Adult numbers were also monitored through BG-S traps. Changes in Wolbachia frequency were compared across hamlets or house blocks.

Results: Releases of adult wMelPop-Ae. aegypti resulted in the transient invasion of wMelPop in all three field sites. Invasion at the Australian sites was heterogeneous, reflecting a slower rate of invasion in locations where background mosquito numbers were high. In contrast, invasion across Tri Nguyen was relatively uniform. After cessation of releases, the frequency of wMelPop declined in all sites, most rapidly in Babinda and Tri Nguyen. Within Machans Beach the rate of decrease varied among areas, and wMelPop was detected for several months in an area with a relatively low mosquito density.

Conclusions: These findings highlight challenges associated with releasing Wolbachia-Ae. aegypti combinations with low fitness, albeit strong virus interference properties, as a means of sustainable control of dengue virus transmission.
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http://dx.doi.org/10.1186/s13071-015-1174-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4625535PMC
October 2015

An outbreak of influenza A(H1N1)pdm09 virus in a primary school in Vietnam.

BMC Res Notes 2015 Oct 15;8:572. Epub 2015 Oct 15.

World Health Organization, Hanoi, Vietnam.

Background: Despite school pupils being at greatest risk during the 2009 influenza pandemic there are limited data on outbreaks of influenza A(H1N1)pdm09 in primary schools in South-East Asia. This prospective cohort study describes an outbreak of influenza A(H1N1)pdm09 in a primary school in rural Vietnam.

Findings: In total 103 cases of influenza-like illness were found among the 407 pupils in the primary school. Ten of these were laboratory confirmed cases of influenza A(H1N1)pdm09 virus. The overall attack rate (AR) was 25% (103/407), and was highest (41%) in grade 4 pupils, where the outbreak started. All cases in the outbreak presented with a mild and self-limiting illness, acute respiratory symptoms and fever. Public health interventions to contain the outbreak could explain the lower attack rates in other grades. Ill pupils were asked to stay at home. Oseltamivir was not given to pupils and the school did not close during the outbreak. The last detected case occurred 12 days following identification of the first case.

Conclusions: This is the first report of an outbreak of influenza A(H1N1)pdm09 among pupils in a primary school in Vietnam. High attack rates in Grade 4 pupils suggest shared activities contributed to transmission. The public health response using non-pharmaceutical measures may have played a role in ending the outbreak.
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http://dx.doi.org/10.1186/s13104-015-1551-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4608302PMC
October 2015

Region-wide synchrony and traveling waves of dengue across eight countries in Southeast Asia.

Proc Natl Acad Sci U S A 2015 Oct 5;112(42):13069-74. Epub 2015 Oct 5.

Department of Biology, University of Florida, Gainesville, FL 32610; Emerging Pathogens Institute, University of Florida, Gainesville, FL 32610.

Dengue is a mosquito-transmitted virus infection that causes epidemics of febrile illness and hemorrhagic fever across the tropics and subtropics worldwide. Annual epidemics are commonly observed, but there is substantial spatiotemporal heterogeneity in intensity. A better understanding of this heterogeneity in dengue transmission could lead to improved epidemic prediction and disease control. Time series decomposition methods enable the isolation and study of temporal epidemic dynamics with a specific periodicity (e.g., annual cycles related to climatic drivers and multiannual cycles caused by dynamics in population immunity). We collected and analyzed up to 18 y of monthly dengue surveillance reports on a total of 3.5 million reported dengue cases from 273 provinces in eight countries in Southeast Asia, covering ∼ 10(7) km(2). We detected strong patterns of synchronous dengue transmission across the entire region, most markedly during a period of high incidence in 1997-1998, which was followed by a period of extremely low incidence in 2001-2002. This synchrony in dengue incidence coincided with elevated temperatures throughout the region in 1997-1998 and the strongest El Niño episode of the century. Multiannual dengue cycles (2-5 y) were highly coherent with the Oceanic Niño Index, and synchrony of these cycles increased with temperature. We also detected localized traveling waves of multiannual dengue epidemic cycles in Thailand, Laos, and the Philippines that were dependent on temperature. This study reveals forcing mechanisms that drive synchronization of dengue epidemics on a continental scale across Southeast Asia.
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http://dx.doi.org/10.1073/pnas.1501375112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4620875PMC
October 2015

Role of Aedes aegypti and Aedes albopictus during the 2011 dengue fever epidemics in Hanoi, Vietnam.

Asian Pac J Trop Med 2015 Jul 9;8(7):543-8. Epub 2015 Jul 9.

National Institute of Hygiene and Epidemiology, 1 Yersin Street, 10000 Hanoi, Viet Nam.

Objective: To record the human cases of dengue fever (DF) and investigate the Aedes mosquito species circulating during the Hanoi 2011 DF epidemics.

Methods: 24 different outbreak points were recorded in 8 districts between August and December 2011.

Results: 140 patients were hospitalized following dengue diagnostic with a predominance of males (59.3%) and the 15-34 age class. Only DENV-1 (11.27%) and DENV-2 (88.73%) serotypes were detected in human samples. Mosquito sampling performed in and around patients households revealed the predominance of Aedes aegypti (A. aegypti) (95.15%) versus Aedes albopictus (4.85%).

Conclusions: There is a positive correlation between the population density of A. aegypti and the number of human cases and duration of outbreaks. This was not observed for Aedes albopictus. Three pools of A. aegypti were positive with dengue virus, two with DENV-1 and one with DENV-2.
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http://dx.doi.org/10.1016/j.apjtm.2015.06.009DOI Listing
July 2015

A model immunization programme to control Japanese encephalitis in Viet Nam.

J Health Popul Nutr 2015 Mar;33(1):207-13

International Vaccine Institute, San 4-8, Bongcheon-7 dong, Kwanak-ku, Seoul 151-818, Republic of Korea ; Department of Epidemiology, Fudan University School of Public Health, Shanghai, China.

In Viet Nam, an inactivated, mouse brain-derived vaccine for Japanese encephalitis (JE) has been given exclusively to ≤ 5 years old children in 3 paediatric doses since 1997. However, JE incidence remained high, especially among children aged 5-9 years. We conducted a model JE immunization programme to assess the feasibility and impact of JE vaccine administered to 1-9 year(s) children in 3 standard-dose regimen: paediatric doses for children aged <3 years and adult doses for those aged ≥ 3 years. Of the targeted children, 96.2% were immunized with ≥ 2 doses of the vaccine. Compared to the national immunization programme, JE incidence rate declined sharply in districts with the model programme (11.32 to 0.87 per 100,000 in pre-versus post-vaccination period). The rate of reduction was most significant in the 5-9 years age-group. We recommend a policy change to include 5-9 years old children in the catch-up immunization campaign and administer a 4th dose to those aged 5-9 years, who had received 3 doses of the vaccine during the first 2-3 years of life.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4438663PMC
March 2015

Differences in the Epidemiology of Human Cases of Avian Influenza A(H7N9) and A(H5N1) Viruses Infection.

Clin Infect Dis 2015 Aug 4;61(4):563-71. Epub 2015 May 4.

Division of Infectious Disease, Key Laboratory of Surveillance and Early-warning on Infectious Disease, Chinese Center for Disease Control and Prevention, Beijing, China.

Background: The pandemic potential of avian influenza viruses A(H5N1) and A(H7N9) remains an unresolved but critically important question.

Methods: We compared the characteristics of sporadic and clustered cases of human H5N1 and H7N9 infection, estimated the relative risk of infection in blood-related contacts, and the reproduction number (R).

Results: We assembled and analyzed data on 720 H5N1 cases and 460 H7N9 cases up to 2 November 2014. The severity and average age of sporadic/index cases of H7N9 was greater than secondary cases (71% requiring intensive care unit admission vs 33%, P = .007; median age 59 years vs 31, P < .001). We observed no significant differences in the age and severity between sporadic/index and secondary H5N1 cases. The upper limit of the 95% confidence interval (CI) for R was 0.12 for H5N1 and 0.27 for H7N9. A higher proportion of H5N1 infections occurred in clusters (20%) compared to H7N9 (8%). The relative risk of infection in blood-related contacts of cases compared to unrelated contacts was 8.96 for H5N1 (95% CI, 1.30, 61.86) and 0.80 for H7N9 (95% CI, .32, 1.97).

Conclusions: The results are consistent with an ascertainment bias towards severe and older cases for sporadic H7N9 but not for H5N1. The lack of evidence for ascertainment bias in sporadic H5N1 cases, the more pronounced clustering of cases, and the higher risk of infection in blood-related contacts, support the hypothesis that susceptibility to H5N1 may be limited and familial. This analysis suggests the potential pandemic risk may be greater for H7N9 than H5N1.
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http://dx.doi.org/10.1093/cid/civ345DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4542598PMC
August 2015

Thirty years of vaccination in Vietnam: Impact and cost-effectiveness of the national Expanded Programme on Immunization.

Vaccine 2015 May;33 Suppl 1:A233-9

National Institute of Hygiene and Epidemiology, Hanoi, Vietnam.

Introduction: Countries like Vietnam transitioning to middle-income status increasingly bear the cost of both existing and new vaccines. However, the impact and cost-effectiveness of the Expanded Programme on Immunization (EPI) as a whole has never been assessed on a country level.

Methods: Data on vaccine-preventable disease incidence and mortality from Vietnam's national surveillance was analysed to estimate the likely impact that vaccination in 1980-2010 may have had. Adjustment for under-reporting was made by examining trends in reported mumps incidence and in case-fatality risks for each disease. The same data were separately analysed using the Lives Saved Tool (LiST) to give an alternative estimate of impact. The financial cost of EPI in 1996-2010 was also estimated from the perspective of service provider.

Results: National surveillance data suggests that up to 5.7 million diseases cases and 26,000 deaths may have been prevented by EPI. Analysis using LiST suggests that even more deaths (370,000) may have been prevented by measles and pertussis vaccination alone. The cost-effectiveness of EPI is estimated to be around $1000-$27,000 per death prevented.

Conclusion: Two separate approaches to assessing EPI impact in Vietnam give different quantitative results but a common conclusion: that EPI has made a substantial impact on mortality and represents good value for money.
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http://dx.doi.org/10.1016/j.vaccine.2014.12.017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4428532PMC
May 2015

Hemagglutination inhibiting antibodies and protection against seasonal and pandemic influenza infection.

J Infect 2015 Feb 16;70(2):187-96. Epub 2014 Sep 16.

Oxford University Clinical Research Unit and Wellcome Trust Major Overseas Programme, Viet Nam; Center for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK.

Objectives: Hemagglutination inhibiting (HI) antibodies correlate with influenza vaccine protection but their association with protection induced by natural infection has received less attention and was studied here.

Methods: 940 people from 270 unvaccinated households participated in active ILI surveillance spanning 3 influenza seasons. At least 494 provided paired blood samples spanning each season. Influenza infection was confirmed by RT-PCR on nose/throat swabs or serum HI assay conversion.

Results: Pre-season homologous HI titer was associated with a significantly reduced risk of infection for H3N2 (OR 0.61, 95%CI 0.44-0.84) and B (0.65, 95%CI 0.54-0.80) strains, but not H1N1 strains, whether re-circulated (OR 0.90, 95%CI 0.71-1.15), new seasonal (OR 0.86, 95%CI 0.54-1.36) or pandemic H1N1-2009 (OR 0.77, 95%CI 0.40-1.49). The risk of seasonal and pandemic H1N1 decreased with increasing age (both p < 0.0001), and the risk of pandemic H1N1 decreased with prior seasonal H1N1 (OR 0.23, 95%CI 0.08-0.62) without inducing measurable A/California/04/2009-like titers.

Conclusions: While H1N1 immunity was apparent with increasing age and prior infection, the effect of pre-season HI titer was at best small, and weak for H1N1 compared to H3N2 and B. Antibodies targeting non-HI epitopes may have been more important mediators of infection-neutralizing immunity for H1N1 compared to other subtypes in this setting.
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http://dx.doi.org/10.1016/j.jinf.2014.09.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4309889PMC
February 2015

Determinants of influenza transmission in South East Asia: insights from a household cohort study in Vietnam.

PLoS Pathog 2014 Aug 21;10(8):e1004310. Epub 2014 Aug 21.

Oxford University Clinical Research Unit - Wellcome Trust Major Overseas Programme, Hanoi, Vietnam.

To guide control policies, it is important that the determinants of influenza transmission are fully characterized. Such assessment is complex because the risk of influenza infection is multifaceted and depends both on immunity acquired naturally or via vaccination and on the individual level of exposure to influenza in the community or in the household. Here, we analyse a large household cohort study conducted in 2007-2010 in Vietnam using innovative statistical methods to ascertain in an integrative framework the relative contribution of variables that influence the transmission of seasonal (H1N1, H3N2, B) and pandemic H1N1pdm09 influenza. Influenza infection was diagnosed by haemagglutination-inhibition (HI) antibody assay of paired serum samples. We used a Bayesian data augmentation Markov chain Monte Carlo strategy based on digraphs to reconstruct unobserved chains of transmission in households and estimate transmission parameters. The probability of transmission from an infected individual to another household member was 8% (95% CI, 6%, 10%) on average, and varied with pre-season titers, age and household size. Within households of size 3, the probability of transmission from an infected member to a child with low pre-season HI antibody titers was 27% (95% CI 21%-35%). High pre-season HI titers were protective against infection, with a reduction in the hazard of infection of 59% (95% CI, 44%-71%) and 87% (95% CI, 70%-96%) for intermediate (1∶20-1∶40) and high (≥1∶80) HI titers, respectively. Even after correcting for pre-season HI titers, adults had half the infection risk of children. Twenty six percent (95% CI: 21%, 30%) of infections may be attributed to household transmission. Our results highlight the importance of integrated analysis by influenza sub-type, age and pre-season HI titers in order to infer influenza transmission risks in and outside of the household.
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http://dx.doi.org/10.1371/journal.ppat.1004310DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4140851PMC
August 2014

Investigation of dengue and Japanese encephalitis virus transmission in Hanam, Viet Nam.

Am J Trop Med Hyg 2014 May 10;90(5):892-896. Epub 2014 Mar 10.

This study investigated whether a large dengue epidemic that struck Hanoi in 2009 also affected a nearby semirural area. Seroconversion (dengue virus-reactive immunoglobulin G enzyme-linked immunosorbent assay) was high during 2009 compared with 2008, but neutralization assays showed that it was caused by both dengue virus and Japanese encephalitis virus infections. The findings highlight the importance of continued Japanese encephalitis virus vaccination and dengue surveillance.
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http://dx.doi.org/10.4269/ajtmh.13-0077DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4015583PMC
May 2014

Pandemic H1N1 virus transmission and shedding dynamics in index case households of a prospective Vietnamese cohort.

J Infect 2014 Jun 1;68(6):581-90. Epub 2014 Feb 1.

Oxford University Clinical Research Unit and Wellcome Trust Major Overseas Programme, Viet Nam; Center for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK; Department of Microbiology and Immunology, University of Melbourne, Australia. Electronic address:

Objectives: Influenza household transmission studies are required to guide prevention strategies but most passively recruit index cases that seek healthcare. We investigated A(H1N1)pdm09 transmission in a household-based cohort during 2009.

Methods: Health-workers visited 270 households weekly, and collected swabs from influenza-like-illness cases. If A(H1N1)pdm09 was RT-PCR-confirmed, all household members had symptoms assessed and swabs collected daily for 10-15 days. Viral RNA was quantified and sequenced and serology performed on pre-pandemic sera.

Results: Index cases were detected in 20 households containing 81 people. 98.5% lacked A(H1N1)pdm09 neutralizing antibodies in pre-pandemic sera. Eleven (18.6%, 95% CI 10.7-30.4%) of 59 contacts were infected. Virus genetic diversity within households was negligible and less than between households. Index and secondary cases were distributed between mothers, daughters and sons, and had similar virus-RNA shedding and symptom dynamics. Fathers were rarely infected. Five secondary cases (45%) had no apparent symptoms and three shed virus before symptoms. Secondary infection was associated with index case wet cough (OR 1.56, 95% CI 1.22-1.99).

Conclusions: In this cohort of A(H1N1)pdm09 susceptible persons, virus sequencing was capable of discriminating household from community transmission. Household transmission involved mothers and children but rarely fathers. Asymptomatic or pre-symptomatic shedding was common.
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http://dx.doi.org/10.1016/j.jinf.2014.01.008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4031397PMC
June 2014

Effectiveness of the Viet Nam produced, mouse brain-derived, inactivated Japanese encephalitis vaccine in Northern Viet Nam.

PLoS Negl Trop Dis 2012 13;6(12):e1952. Epub 2012 Dec 13.

International Vaccine Institute, Seoul, South Korea.

Background: Japanese encephalitis (JE) is a flaviviral disease of public health concern in many parts of Asia. JE often occurs in large epidemics, has a high case-fatality ratio and, among survivors, frequently causes persistent neurological sequelae and mental disabilities. In 1997, the Vietnamese government initiated immunization campaigns targeting all children aged 1-5 years. Three doses of a locally-produced, mouse brain-derived, inactivated JE vaccine (MBV) were given. This study aims at evaluating the effectiveness of Viet Nam's MBV.

Methodology: A matched case-control study was conducted in Northern Viet Nam. Cases were identified through an ongoing hospital-based surveillance. Each case was matched to four healthy controls for age, gender, and neighborhood. The vaccination history was ascertained through JE immunization logbooks maintained at local health centers.

Principal Findings: Thirty cases and 120 controls were enrolled. The effectiveness of the JE vaccine was 92.9% [95% CI: 66.6-98.5]. Confounding effects of other risk variables were not observed.

Conclusions: Our results strongly suggest that the locally-produced JE-MBV given to 1-5 years old Vietnamese children was efficacious.
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http://dx.doi.org/10.1371/journal.pntd.0001952DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3521705PMC
May 2013