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Seroincidence of Influenza Among HIV-infected and HIV-uninfected Men Who Have Sex with Men During the 2009 H1N1 Influenza Pandemic in Bangkok, Thailand

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  • Armed Forces Research Institute of Medical Sciences, AFRIMS

Abstract and Figures

Among 368 Thai men who have sex with men with paired serum samples collected before and during the 2009 H1N1 influenza pandemic, we determined influenza A (H1N1)pdm09 seroconversion rates (≥4-fold rise in antibody titers by hemagglutination inhibition or microneutralization assays). Overall, 66 of 232 (28%) participants seroconverted after the first year of A(H1N1)pdm09 activity, and 83 of 234 (35%) participants seroconverted after the second year. Influenza A(H1N1)pdm09 seroconversion did not differ between human immunodeficiency virus (HIV)-infected (55 of 2157 [35%]) and HIV-uninfected (71 of 2211 [34%]) participants (P = .78). Influenza A(H1N1)pdm09 seroconversion occurred in approximately one third of our Thai study population and was similar among HIV-infected and HIV-uninfected participants.
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BRIEF REPORT
Seroincidence of Inuenza Among
HIV-infected and HIV-uninfected
Men During the 2009 H1N1
Inuenza Pandemic, Bangkok,
Thailand
Shikha Garg,1Sonja J. Olsen,2,3 Stefan Fernandez,4Charung Muangchana,5
Kamonthip Rungrojcharoenkit,4Prabda Prapasiri,3Jacqueline M. Katz,2
Marcel E. Curlin,1,3 Robert V. Gibbons,4Timothy H. Holtz,1,3
Anupong Chitwarakorn,6and Fatimah S. Dawood2
1
Division of HIV/AIDS Prevention and
2
Inuenza Division, Centers for Disease
Control and Prevention, Atlanta, Georgia;
3
Thailand MoPH-U.S. CDC Collaboration,
Nonthaburi;
4
Armed Forces Research Institute of Medical Sciences, Bangkok,
5
National Vaccine Institute, Nonthaburi, and
6
Department of Disease Control,
Ministry of Public Health, Thailand
Among 368 Thai men who have sex with men with paired
serum samples collected before and during the 2009 H1N1
inuenza pandemic, we determined inuenza A (H1N1)
pdm09 seroconversion rates (4-fold rise in antibody titers
by hemagglutination inhibition or microneutralization as-
says). Overall, 66 of 232 (28%) participants seroconverted
after the rst year of A(H1N1)pdm09 activity, and 83 of
234 (35%) participants seroconverted after the second year.
Inuenza A(H1N1)pdm09 seroconversion did not differ be-
tween human immunodeciency virus (HIV)-infected (55 of
2157 [35%]) and HIV-uninfected (71 of 2211 [34%]) partic-
ipants (P=.78). Inuenza A(H1N1)pdm09 seroconversion
occurred in approximately one third of our Thai study pop-
ulation and was similar among HIV-infected and HIV-unin-
fected participants.
Keywords.A(H1N1)pdm09; HIV; inuenza; pandemic;
serology; Thailand.
In April 2009, the inuenza A (H1N1)pdm09 virus emerged
and rapidly gave rise to the rst inuenza pandemic in 40
years [1]. Serologic surveys have been used to estimate cumula-
tive incidence of infection in populations worldwide. A recent
global meta-analysis of A(H1N1)pdm09 serologic surveys esti-
mated an overall incidence of 20% in the rst year of virus cir-
culation, with substantial variation across age groups and
regions [2]. Because most serologic surveys were based on sam-
ples of the general population, data remain limited on the inci-
dence of A(H1N1)pdm09 infection among persons with
underlying conditions associated with an increased risk for se-
vere inuenza, particularly from developing countries.
Human immunodeciency virus (HIV) infection increases
the risk of severe illness and complications from inuenza
[35], although it is unknown whether HIV infection increases
susceptibility to inuenza. Data on A(H1N1)pdm09 infection
in persons infected with HIV are largely limited to studies
from developed countries. Understanding the impact of inu-
enza pandemics and whether susceptibility differs among per-
sons with and without HIV infection could inform global and
national prioritization strategies for inuenza vaccination, par-
ticularly early in an inuenza pandemic when global vaccine
supply is likely to be limited.
In Thailand, the rst laboratory-conrmed cases of A(H1N1)
pdm09infection occurredin the rst week of May 2009. Emergence
of the virus subsequently resulted in 3 distinct waves of circulation
during the rst 2 years after being identied in the population (Fig-
ure 1)[6]. The A(H1N1)pdm09 monovalent vaccine became avail-
able in Thailand in January 2010, and access to the vaccine was
limited with only 2 million doses purchased by the government
(Thai population, 66 million). Access to seasonal inuenza vaccine
was also limited in Thailand [7]. We estimated the strain-specic
incidence of inuenza among a cohort of Thai men who have sex
with men (MSM) with and without HIV infection in Bangkok.
METHODS
Setting
Men who have sex with men residing in Bangkok were enrolled
into the Bangkok Mens Cohort Study (BMCS) starting in April
2006 as part of an ongoing study to estimate HIV incidence [8].
Serum specimens were collected from BMCS participants at en-
rollment and every 4 months for those with HIV infection and
every 12 months for those without. The BMCS participants
consented to storage of specimens for future testing at enroll-
ment. This study was approved by the Institutional Review
Board at the Centers for Disease Control and Prevention and
the Ministry of Public Health, Thailand.
Received 5 June 2014; accepted 11 August 2014.
Correspondence: Fatimah S. Dawood, MD, Centers for Disease Control and Prevention, 1600
Clifton Road, Mailstop A32, Atlanta, GA 30333 (hgj0@cdc.gov).
Open Forum Infectious Diseases
© The Author 2014. Published by Oxford University Press on beh alf of the Infectious Diseases
Society of Americ a. This is an Ope n Access artic le distributed under the ter ms of the Creative
Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/lic enses/
by-nc-nd/4.0/), which permit s non-commercial reproduction and distribution of the work, in any
medium, provided the original work is not al tered or transformed in any way, and that the work
is properly cited. For commercial re-use, please contact journals.permissions@ oup.com.
DOI: 10.1093/od/ofu082
BRIEF REPORT OFID 1
Specimen Selection
Stored serum specimens were selected from BMCS participants
who had blood drawn at least once during May 2008May 2009
and at least once during AprilJuly 2010 or JanuaryMarch
2011. These time points were chosen to obtain baseline serum
specimens before A(H1N1)pdm09 circulation in Thailand and
follow-up serum specimens either after the rst 2 waves or third
wave of A(H1N1)pdm09 circulation (Figure 1)[6]. For partic-
ipants who had serum specimens available at all 3 time points,
paired specimens for after the rst waves and after the third
wave of the pandemic were treated independently.
Laboratory Testing
Serum was tested by hemagglutination inhibition (HI)
assays using guinea pig erythrocytes for antibody response to
A/California/08/2009, A/Brisbane/59/2007, A/Perth/16/2009,
and B/Brisbane/60/2008 and by microneutralization (MN) as-
says against A/California/08/2009. Specimens were tested at
the Armed Forces Research Institute of Medical Science in
Bangkok, Thailand using the standard World Health Organiza-
tion protocol [9,10]. For A(H1N1)pdm09, seroconversion was
dened as 4-fold rise in HI or MN antibody titers and a min-
imum titer on the second sample of 40. For all other virus types
and subtypes, seroconversion was dened as 4-fold rise in HI
antibody titers only and a minimum HI titer on the second
sample of 40. Because several studies have suggested that a min-
imal titer of 20 may be optimal for assessing seroconversion to
novel viruses, we also assessed A(H1N1)pdm09 seroconversion
based on a minimal titer on the second sample of 20 [11,12]. If a
baseline titer was <10 (lower limit of detection), the titer was set
equal to 5 for analytic purposes. Human immunodeciency
virus testing methods for the BMCS have been previously de-
scribed [8]. Although access to inuenza vaccine is limited in
Thailand with <5% coverage in high-risk groups in 2010 and
2011, it is not known whether BMCS participants received in-
uenza vaccine before baseline serum collection.
Sample Size Calculation
The BMCS contains 500 participants infected with HIV and
1000 HIV-uninfected (negative for HIV at the time of the rst
sample collection) participants. To obtain representative esti-
mates of inuenza seroincidence among HIV-infected and
HIV-uninfected participants separately in the BMCS, we need-
ed paired serum samples from a minimum of 141 HIV-infected
persons and 164 HIV-uninfected persons after the rst 2 waves
and after the third wave of the pandemic. These calculations
were based on an assumption of a type I error of 5%, an expect-
ed cumulative A(H1N1)pdm09 inuenza incidence of 15%, and
5% precision.
Analysis
We calculated the proportion of HIV-infected and HIV-unin-
fected participants who seroconverted after the rst 2 waves
or after the third wave of the pandemic; participants with spec-
imens collected at all 3 time points were included in both anal-
yses. To increase our sample size and allow for comparisons
Figure 1. The 3 waves of the 2009 H1N1 inuenza pandemic in Thailand based on national Thai surveillance of inuenza-like illness, laboratory-
conrmed cases of A(H1N1)pdm09 and A(H1N1)pdm09-associated deaths (reproduced with permission from Siriraj Med J. 2011;64).
2OFID BRIEF REPORT
between HIV-infected and HIV-uninfected participants, we
used χ
2
tests to compare the proportion of participants who se-
roconverted at any time point for each of the circulating inu-
enza types or subtypes. Participants with specimens collected at
all 3 time points were counted only once. Tests were 2-tailed,
and a Pvalue of .05 was considered signicant. Analyses were
conducted using SAS, version 9.2 (SAS Institute, Cary, North
Carolina).
RESULTS
Paired serum samples were available for 368 participants (157
HIV-infected and 211 HIV-uninfected). The BMCS members
included in our study did not differ from those not included
in our study based on age. Among the 157 HIV-infected men
who had samples available from before the pandemic, 61 had
paired samples available after the rst 2 waves, 46 after the
third wave of the pandemic, and 50 after both the rst 2
waves and the third wave of the pandemic. Among the 211
HIV-uninfected men who had samples from before the pan-
demic, 73 had paired samples available after the rst 2 waves,
90 after the third wave, and 48 after both the rst 2 waves
and the third wave of the pandemic (Figure 2).
At the time the rst serum sample was drawn, the median age
of HIV-infected men was 28 years (range: 1949 years), and the
median age of HIV-uninfected men was 28 years (range: 1955
years). Among the 157 HIV-infected men, 8 (5%) had CD4 cell
counts <200 cells/mm
3
, 32 (21%) had CD4 cell counts of 200
350 cells/mm
3
, and 116 (74%) had CD4 cell counts >350 cells/
mm
3
. No individuals had a CD4 cell count <50 cells/mm
3
. The
median plasma HIV viral load was 28 900 copies/mL (range:
01 480 000 copies/mL). Human immunodeciency virus viral
load was <47 copies/mL (lower limit of detection) in 4 (3%)
men infected with HIV. Only 19 (12%) men were on antiretro-
viral therapy. Among the 211 men who were HIV-uninfected at
the rst serum sample collection, 60 (28%) seroconverted to
HIV-infected during the study.
Four inuenza virus types and subtypes circulated during the
study period: A(H1N1), A(H1N1)pdm09, A(H3N2), and B vi-
ruses. Among HIV-infected men, seroconversion by HI against
any inuenza virus type or subtype was found in 14 of 111
(13%) after the rst 2 waves and 12 of 96 (12%) after the third
wave of the pandemic. Among HIV-uninfected men, serocon-
version by HI against any inuenza virus was found in 12 of 121
(10%) after the rst 2 waves and 16 of 138 (12%) after the third
wave of the pandemic (Table 1).
Among HIV-infected men, cumulative A(H1N1)pdm09
seroincidence was 30 of 111 (27%) after the rst 2 waves and
35 of 96 (36%) after the third wave of the pandemic based on
HI or MN. Among HIV-uninfected men, cumulative A(H1N1)
pdm09 seroincidence was 36 of 121 (30%) after the rst 2 waves
and 48 of 138 (35%) after the third wave of the pandemic based on
HI or MN. Cumulative A(H1N1)pdm09 seroincidence at any
time point was similar among HIV-infected and HIV-uninfected
Figure 2. Inuenza serology testing among BMCS participants with stored serum samples available before and after the rst 2 waves and third wave of
the 2009 H1N1 inuenza pandemic. Abbreviations: BMCS, Bangkok Mens Cohort Study; HIV, human immunodeciency virus.
BRIEF REPORT OFID 3
MSM based on HI alone, MN alone, or HI or MN (Table 1).
When the minimal titer required for seroconversion on the sec-
ond sample was lowered to 20, overall seroconversion against A
(H1N1)pdm09 by HI increased from 10 (4%) to 31 (13%) after
the rst 2 waves and 12 (5%) to 46 (20%) after the third wave.
BasedonHItesting,2(0.5%)menhadbaselineA(H1N1)
pdm09 antibody titers 40. Based on MN testing, 91 (25%)
men had baseline A(H1N1)pdm09 antibody titers 40.
In a subanalysis of 61 men who were classied as HIV-unin-
fected but who seroconverted to HIV-infected during the study,
the cumulative A(H1N1)pdm09 seroincidence was 12 of 38
(32%) after the rst 2 waves and 18 of 55 (33%) after the
third wave of the pandemic based on HI or MN.
DISCUSSION
Among Thai MSM participating in the BMCS, approximately
one third seroconverted to A(H1N1)pdm09 during the rst 3
waves of the A(H1N1)pdm09 pandemic, roughly corresponding
to the rst 2 years of A(H1N1)pdm09 circulation in Thailand.
HIV infection did not increase the risk of seroconversion in our
study population, in which the majority of men had CD4 cell
counts >200 cells/mm
3
. The cumulative seroincidence of sea-
sonal inuenza viruses was similar to A(H1N1)pdm09 during
the rst 3 waves of the pandemic, highlighting the added bur-
den of seasonal inuenza in Thailand during the pandemic.
Our ndings show a higher seroincidence of A(H1N1)
pdm09 based on seroconversion by HI or MN than pooled
results from a meta-analysis of 12 studies with paired sera
that estimated a cumulative A(H1N1)pdm09 seroincidence
after the rst year of virus circulation of 20% (range: 13%
26%) among persons aged 2044 years [2]. However, compari-
sons between the seroincidence rates in our study and those of
other studies should be made with caution because most pub-
lished studies on A(H1N1)pdm09 seroincidence were based
largely on studies using HI alone [2]. In comparison to our nd-
ings, another Thai study that estimated A(H1N1)pdm09 infec-
tion rates in various populations after the rst wave of the
pandemic using an HI titer 40 found infection rates of 3%
in adults in the general population, consistent with our nding
of an A(H1N1)pdm09 seroincidence of 4% after the rst wave
of the pandemic based on HI alone [13]. Although using a min-
imal HI titer of 40 as a marker of immunity is standard for se-
rologic studies, several studies have found that in polymerase
chain reaction-conrmed inuenza A(H1N1)pdm09 infections,
the optimal HI titer cut-off value was 20 for identifying persons
with prior infection [11,12]; this lower cutoff increased the pos-
itivity of our HI assay 3- to 4-fold and may more accurately re-
ect true seroconversion rates by HI.
Table 1. Inuenza Seroincidence by Hemagglutination Inhibition and Microneutralization Assay After the First Two Waves,
a
After the
Third Wave,
b
and After the First Two Waves or Third Wave of the 2009 H1N1 Inuenza Pandemic Among HIV-Infected and HIV-Uninfected
Men Who Have Sex With Men: Bangkok, Thailand, 20092011
Influenza Virus Type/
Subtype
Influenza Seroincidence
Overall (n= 368); no. (%)
Influenza Seroincidence
Among HIV-Infected MSM
(n= 157); no. (%)
Influenza Seroincidence
Among HIV-uninfected MSM
(n= 211); no. (%)
P
Value
c
1st 2
Waves
(n= 232)
3rd Wave
(n= 234)
1st 2
Waves or
3rd Wave
(n= 368)
1st 2
Waves
(n= 111)
3rd
Wave
(n= 96)
1st 2
Waves or
3rd Wave
(n= 157)
1st 2
Waves
(n= 121)
3rd Wave
(n= 138)
1st 2
Waves or
3rd Wave
(n= 211)
Seroincidence by HI
A (H1N1)pdm09 10 (4) 12 (5) 18 (5) 6 (5) 6 (6) 11 (7) 4 (3) 6 (4) 7 (3) 0.10
A (H1N1) 8 (3) 9 (4) 15 (4) 4 (4) 3 (3) 6 (4) 4 (3) 6 (4) 9 (4) 0.83
A (H3N2) 4 (2) 8 (3) 12 (3) 2 (2) 3 (3) 5 (3) 2 (2) 5 (4) 7 (3) 0.94
B 7 (3) 7 (3) 13 (4) 4 (4) 2 (2) 5 (3) 3 (2) 5 (4) 8 (4) 0.76
Any influenza
virus type
26 (11) 28 (12) 47 (13) 14 (13) 12 (12) 23 (15) 12 (10) 16 (12) 24 (11) 0.35
Seroincidence by MN
A (H1N1)pdm09 66 (28) 83 (35) 126 (34) 30 (27) 35 (36) 55 (35) 36 (30) 48 (35) 71 (33) 0.78
Seroincidence by HI or MN
A (H1N1)pdm09 66 (28) 83 (35) 126 (34) 30 (27) 35 (36) 55 (35) 36 (30) 48 (35) 71 (34) 0.78
Abbreviations: HI, hemagglutination inhibition; HIV, human immunodeficiency virus; MN, microneutralization assay; MSM, men who have sex with men.
a
Time period after the second wave of the pandemic: April 1, 2010July 31, 2010.
b
Time period after the third wave of the pandemic: January 1, 2011March 31, 2011.
c
Based on comparison of influenza seroincidence after first 2 waves or third wave of pandemic combined among HIV-infected and HIV-uninfected MSM.
4OFID BRIEF REPORT
Data on A(H1N1)pdm09 seroincidence among individuals
infected with HIV are limited. We found no differences in A
(H1N1)pdm09 seroincidence among HIV-infected and HIV-
uninfected MSM. Likewise, a US study comparing HIV-infected
women with CD4 cell counts 350 cells/mm
3
and HIV-unin-
fected women found no differences in A(H1N1)pdm09 seroin-
cidence [14]. A Taiwanese study comparing HIV-infected and
HIV-uninfected men also found no difference in A(H1N1)
pdm09 seroconversion based on HI [15]. In Australia, A
(H1N1)pdm09 seroprevalence among HIV-infected persons
based on single serum samples was similar to national seropre-
valence estimates, and results were not different based on CD4
cell count or HIV viral load [16]. Although our study and prior
studies suggest that HIV infection does not confer an increased
susceptibility to inuenza virus infection, HIV-infected persons
in these studies were not severely immunocompromised, mak-
ing it difcult to draw conclusions about risk among HIV-
infected persons with low CD4 cell counts. It is possible that
individuals infected with HIV were unable to mount detect-
able antibody responses after inuenza infection due to B-cell
dysfunction [17], thus accounting for the lack of differences in
susceptibility to inuenza infection seen among HIV-infected
and HIV-uninfected individuals. However, the fact that seroin-
cidence was similar among HIV-infected and HIV-uninfected
individuals rather than higher among HIV-uninfected individ-
uals would suggest that HIV-infected individuals do mount a
detectable antibody response to inuenza infection. Prior stud-
ies have demonstrated that HIV infection confers an increased
risk for severe inuenza infection, supporting the importance of
targeted inuenza vaccination among persons infected with
HIV [18].
Several points should be considered when interpreting our
ndings. First, one quarter of men had elevated titers to A
(H1N1)pdm09 at baseline based on MN, whereas only 0.5%
of men had elevated baseline titers based on HI. The MN nd-
ings may suggest that Thai adults had relatively high levels of
preexisting cross-reactive antibody to A(H1N1)pdm09 from
prior infection with other inuenza viruses [19]. However, de-
tection of cross-reactive antibodies to previously circulating in-
uenza strains by MN is unlikely to have impacted our results
because we dened A/H1N1pdm09 infection as evidence of a 4-
fold rise in A(H1N1)pdm09 antibody titers using paired sera
rather than as a single titer of 40, as some prior studies have
done based on HI testing results. Second, although A(H1N1)
pdm09 seroincidence was similar among HIV-infected and
HIV-uninfected MSM, our study may not have had adequate
power to detect differences in seroincidence by HIV infection
status. Third, A(H1N1)pdm09 seroincidence varies by age
group, and our data reect only seroincidence among younger
adults in Thailand. Strengths of our study include testing of
paired sera to determine seroincidence rather than just seropre-
valence of antibodies to A(H1N1)pdm09 and availability of sera
from several time points allowing estimation of seroincidence
after both the rst and second years of A(H1N1)pdm09 circu-
lation in Thailand.
CONCLUSIONS
As seen in other populations in many countries, a substantial
proportion of Thai MSM in Bangkok seroconverted to
A(H1N1)pdm09 during the 2009 pandemic in the absence of
A(H1N1)pdm09 vaccine and in the setting of limited availabil-
ity of seasonal inuenza vaccine. Although HIV infection did
not appear to increase the probability of A(H1N1)pdm09 sero-
conversion, the majority of HIV-infected MSM in this study
were young and had relatively preserved immune function. It
remains unclear whether severely immunocompromised per-
sons infected with HIV are more susceptible to A(H1N1)
pdm09 inuenza virus and to seasonal inuenza viruses in ge-
neral. Given that persons infected with HIV are at risk for more
complicated illness once infected with inuenza, these individ-
uals should continue to be prioritized for inuenza vaccination
during seasonal inuenza epidemics and pandemics.
Acknowledgments
We thank Marc-Alain Widdowson for assistance with study design and
planning; Wannee Chonwattana for laboratory assistance; Wichuda Sukwicha
and Philip Mock for data management assistance; and Dr. Iamsirithaworn
Sopon for sharing national Thai surveillance data.
Disclaimer. The ndings and conclusions in this article are those of the
authors and do not necessarily represent the views of the Centers for Disease
Control and Prevention or the Department of Defense.
Financial support. This work was supported by the US Centers for Dis-
ease Control and Prevention.
Potential conicts of interest. All authors: No reported conicts.
All authors have submitted the ICMJE Form for Disclosure of Potential
Conicts of Interest.
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6OFID BRIEF REPORT
... Data on seroconversion in response to influenza virus infection in Thailand are scarce; no study has reported seroconversion data for seasonal influenza and most studies of seroconversion to influenza A (H1N1)pdm09 virus during the 2009 influenza pandemic focused on seroconversion in special populations (Lerdsamran et al., 2011;Garg et al., 2014;Khuntirat et al., 2014;Simmerman et al., 2011). For instance, using specimens collected in 2009, Lerdsamran et al. reported a substantial influenza A (H1N1) pdm09 virus-specific infection rate among healthy children aged <15 years old compared to healthy adults (Lerdsamran et al., 2011). ...
... For instance, using specimens collected in 2009, Lerdsamran et al. reported a substantial influenza A (H1N1) pdm09 virus-specific infection rate among healthy children aged <15 years old compared to healthy adults (Lerdsamran et al., 2011). A Thai study by Garg et al. reported influenza A (H1N1)pdm09 seroincidence in the population of men who have sex with men between 2009-2011 (Garg et al., 2014). In our study, the overall incidence of influenza virus infection was high (35 infections per 100 person-years). ...
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... Focusing on the immune response to the swine flu, according to a recent Thai report, it was found that "seroconversion occurred in approximately one third of the patients with swine flu [8]". It is also reported the observed pattern is not different between HIV-infected and HIV-uninfected cases [9]. Of interest, it seems that the clinical feature in HIV seropositive cases is not different from those with seronegativity. ...
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Southeast Asia is a region with great potential for the emergence of a pandemic influenza virus. Global efforts to improve influenza surveillance in this region have documented the burden and seasonality of influenza viruses and have informed influenza prevention strategies, but little information exists about influenza vaccination guidelines and vaccine sales. To ascertain the existence of influenza vaccine guidelines and define the scope of vaccine sales, we sent a standard three-page questionnaire to the ten member nations of the Association of Southeast Asian Nations. We also surveyed three multinational manufacturers who supply influenza vaccines in the region. Vaccine sales in the private sector were <1000 per 100,000 population in the 10 countries. Five countries reported purchasing vaccine for use in the public sector. In 2011, Thailand had the highest combined reported rate of vaccine sales (10,333 per 100,000). In the 10 countries combined, the rate of private sector sales during 2010-2011 (after the A(H1N1)2009pdm pandemic) exceeded 2008 pre-pandemic levels. Five countries (Indonesia, Malaysia, Singapore, Thailand and Vietnam) had guidelines for influenza vaccination but only two were consistent with global guidelines. Four recommended vaccination for health care workers, four for elderly persons, three for young children, three for persons with underlying disease, and two for pregnant women. The rate of vaccine sales in Southeast Asia remains low, but there was a positive impact in sales after the A(H1N1)2009pdm pandemic. Low adherence to global vaccine guidelines suggests that more work is needed in the policy arena.
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Background: The global impact of the 2009 influenza A(H1N1) pandemic (H1N1pdm) is not well understood. Objectives: We estimate overall and age-specific prevalence of cross-reactive antibodies to H1N1pdm virus and rates of H1N1pdm infection during the first year of the pandemic using data from published and unpublished H1N1pdm seroepidemiological studies. Methods: Primary aggregate H1N1pdm serologic data from each study were stratified in standardized age groups and evaluated based on when sera were collected in relation to national or subnational peak H1N1pdm activity. Seropositivity was assessed using well-described and standardized hemagglutination inhibition (HI titers ≥ 32 or ≥ 40) and microneutralization (MN ≥ 40) laboratory assays. The prevalence of cross-reactive antibodies to the H1N1pdm virus was estimated for studies using sera collected prior to the start of the pandemic (between 2004 and April 2009); H1N1pdm cumulative incidence was estimated for studies in which collected both pre- and post-pandemic sera; and H1N1pdm seropositivity was calculated from studies with post-pandemic sera only (collected between December 2009-June 2010). Results: Data from 27 published/unpublished studies from 19 countries/administrative regions - Australia, Canada, China, Finland, France, Germany, Hong Kong SAR, India, Iran, Italy, Japan, Netherlands, New Zealand, Norway, Reunion Island, Singapore, United Kingdom, United States, and Vietnam - were eligible for inclusion. The overall age-standardized pre-pandemic prevalence of cross-reactive antibodies was 5% (95%CI 3-7%) and varied significantly by age with the highest rates among persons ≥ 65 years old (14% 95%CI 8-24%). Overall age-standardized H1N1pdm cumulative incidence was 24% (95%CI 20-27%) and varied significantly by age with the highest in children 5-19 (47% 95%CI 39-55%) and 0-4 years old (36% 95%CI 30-43%). Conclusions: Our results offer unique insight into the global impact of the H1N1 pandemic and highlight the need for standardization of seroepidemiological studies and for their inclusion in pre-pandemic preparedness plans. Our results taken together with recent global pandemic respiratory-associated mortality estimates suggest that the case fatality ratio of the pandemic virus was approximately 0.02%.
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Objective: To assess HIV-prevalence, incidence and risk factors in a cohort of men who have sex with men (MSM) in Bangkok. Design: : Cohort study with 4-monthly follow-up visits conducted between April 2006 and July 2012 at a dedicated study clinic in a central Bangkok hospital. Participants were 1744 homosexually active Thai men, at least 18 years old and residents of Bangkok. Methods: Men were tested for HIV-infection at every study visit and for sexually transmitted infections at baseline. Demographic and behavioural data were collected by audio-computer-assisted self-interview. Logistic regression analysis was used to evaluate risk factors for HIV-prevalence and Cox proportional hazard analysis to evaluate risk factors for HIV-incidence. Results: Baseline HIV-prevalence was 21.3% (n = 372) and 60 months cumulative HIV-incidence was 23.9% (n = 222). Overall HIV-incidence density was 5.9 per 100 person-years. Multivariate risk factors for HIV-prevalence were older age, secondary/vocational education (vs. university or higher), employed or unemployed (vs. studying), nitrate inhalation, drug use for sexual pleasure, receptive anal intercourse, history of sexual coercion, no prior HIV-testing, and anti-HSV-1 and 2 and Treponema pallidum positivity at baseline. Multivariate risk factors for HIV-incidence were younger age, living alone or with roommate (vs. with a partner or family), drug use for sexual pleasure, inconsistent condom use, receptive anal intercourse, group sex, and anti-HSV-1 and 2 and T. pallidum positivity at baseline. Having no anal intercourse partners was inversely associated with HIV-incidence. Conclusion: The high HIV prevalence and incidence in this cohort of Bangkok MSM documents an explosive epidemic. Additional preventive interventions for MSM are urgently needed.
Article
Objective: To describe the clinical course of infection by 2009 (H1N1) influenza virus in different stages of HIV disease. Design: Prospective, observational study. Methods: During the pandemic period, HIV-infected patients presenting respiratory symptoms at a third level referral hospital in Mexico City were tested for 2009 influenza A (H1N1) viral RNA. Clinical files were prospectively analyzed. Results: Infection by H1N1 was confirmed in 30 (23.8%) of the total 126 HIV-infected patients studied. In the group of patients with 2009 H1N1 virus infection, 16 (53.3%) were hospitalized, 12 (40%) had active opportunistic infections and six (20%) died. In the group of 96 patients not infected with 2009 H1N1 virus, 54 (56.25%) were hospitalized with opportunistic infections and 12 (12.5%) died. For all hospitalized patients, being on HAART and having undetectable HIV viral loads at hospitalization was associated with higher survival (P = 0.019). Patients with 2009 H1N1 virus infection had a higher mortality rate, even after adjusting for HAART (P = 0.043). Coinfection by HIV and H1N1 2009 virus was more severe in patients with opportunistic infections, as shown by longer hospital stays (P = 0.0013), higher rates of hospitalization (P < 0.0001), use of mechanical ventilation (P = 0.0086) and death (P = 0.026). Delayed administration of oseltamivir in hospitalized patients was significantly associated with mortality (P = 0.0022). Conclusion: Our data suggest that infection by 2009 H1N1 is more severe in HIV-infected patients with late and advanced HIV disease than in well controlled patients under HAART.
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Background: The seroprevalence and seroincidence of novel influenza A infection among HIV-infected patients, who were believed to have more severe outcomes than healthy individuals, are rarely investigated in the era of highly active antiretroviral therapy (HAART). Our aim was to determine the seroprevalence and seroincidence of novel influenza A infection among HIV-infected patients in Taiwan. Methods: Between September and November 2009, before the implementation of a nationwide vaccination for novel influenza A in Taiwan, 931 HIV-infected patients and 566 persons seeking voluntary counseling and testing (VCT) for HIV infection at our university hospital were enrolled in this study. Antibody responses to novel influenza A were determined using a hemagglutination-inhibition (HI) assay. Results: HIV-infected patients had a significantly lower seroprevalence of novel influenza A infection than VCT clients (14.7% vs. 33.9%, p < 0.001). The seroincidence of novel influenza A infection among HIV-infected patients was 9.4% (95% confidence interval [CI]: 7.6-11.4). On the multivariate analysis, heterosexual (odds ratio [OR]: 1.89; 95% CI: 1.105-3.227) and baseline HI titer (OR: 1.02; 95% CI: 1.001-1.038) were significantly associated with seroconversion to novel influenza A virus. Conclusion: HIV-infected patients demonstrated a lower seroprevalence of novel influenza A infection than HIV-uninfected patients in Taiwan in the HAART era. Among HIV-infected patients, seroconversion to novel influenza A virus, which was infrequent during the 2009 influenza epidemic, was associated with heterosexual behavior and baseline HI titer.