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BRIEF REPORT
Seroincidence of Influenza Among
HIV-infected and HIV-uninfected
Men During the 2009 H1N1
Influenza 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
Influenza 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
influenza pandemic, we determined influenza 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 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 be-
tween human immunodeficiency virus (HIV)-infected (55 of
2157 [35%]) and HIV-uninfected (71 of 2211 [34%]) partic-
ipants (P=.78). Influenza 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; influenza; pandemic;
serology; Thailand.
In April 2009, the influenza A (H1N1)pdm09 virus emerged
and rapidly gave rise to the first influenza 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 first 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 influenza, particularly from developing countries.
Human immunodeficiency virus (HIV) infection increases
the risk of severe illness and complications from influenza
[3–5], although it is unknown whether HIV infection increases
susceptibility to influenza. Data on A(H1N1)pdm09 infection
in persons infected with HIV are largely limited to studies
from developed countries. Understanding the impact of influ-
enza pandemics and whether susceptibility differs among per-
sons with and without HIV infection could inform global and
national prioritization strategies for influenza vaccination, par-
ticularly early in an influenza pandemic when global vaccine
supply is likely to be limited.
In Thailand, the first laboratory-confirmed cases of A(H1N1)
pdm09infection occurredin the first week of May 2009. Emergence
of the virus subsequently resulted in 3 distinct waves of circulation
during the first 2 years after being identified 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 influenza vaccine
was also limited in Thailand [7]. We estimated the strain-specific
incidence of influenza 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 Men’s 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/ofid/ofu082
BRIEF REPORT •OFID •1
Specimen Selection
Stored serum specimens were selected from BMCS participants
who had blood drawn at least once during May 2008–May 2009
and at least once during April–July 2010 or January–March
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 first 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 first 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
defined 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 defined 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 immunodeficiency
virus testing methods for the BMCS have been previously de-
scribed [8]. Although access to influenza 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-
fluenza 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 first
sample collection) participants. To obtain representative esti-
mates of influenza 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 first 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 influenza incidence of 15%, and
5% precision.
Analysis
We calculated the proportion of HIV-infected and HIV-unin-
fected participants who seroconverted after the first 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 influenza pandemic in Thailand based on national Thai surveillance of influenza-like illness, laboratory-
confirmed cases of A(H1N1)pdm09 and A(H1N1)pdm09-associated deaths (reproduced with permission from Siriraj Med J. 2011;64).
2•OFID •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 influ-
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 significant. 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 first 2 waves, 46 after the
third wave of the pandemic, and 50 after both the first 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 first 2 waves,
90 after the third wave, and 48 after both the first 2 waves
and the third wave of the pandemic (Figure 2).
At the time the first serum sample was drawn, the median age
of HIV-infected men was 28 years (range: 19–49 years), and the
median age of HIV-uninfected men was 28 years (range: 19–55
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:
0–1 480 000 copies/mL). Human immunodeficiency 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 first serum sample collection, 60 (28%) seroconverted to
HIV-infected during the study.
Four influenza 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 influenza virus type or subtype was found in 14 of 111
(13%) after the first 2 waves and 12 of 96 (12%) after the third
wave of the pandemic. Among HIV-uninfected men, serocon-
version by HI against any influenza virus was found in 12 of 121
(10%) after the first 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 first 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 first 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. Influenza serology testing among BMCS participants with stored serum samples available before and after the first 2 waves and third wave of
the 2009 H1N1 influenza pandemic. Abbreviations: BMCS, Bangkok Men’s Cohort Study; HIV, human immunodeficiency 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 first 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 classified 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 first 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 first 3
waves of the A(H1N1)pdm09 pandemic, roughly corresponding
to the first 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 influenza viruses was similar to A(H1N1)pdm09 during
the first 3 waves of the pandemic, highlighting the added bur-
den of seasonal influenza in Thailand during the pandemic.
Our findings 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 first year of virus circulation of 20% (range: 13%–
26%) among persons aged 20–44 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 find-
ings, another Thai study that estimated A(H1N1)pdm09 infec-
tion rates in various populations after the first wave of the
pandemic using an HI titer ≥40 found infection rates of 3%
in adults in the general population, consistent with our finding
of an A(H1N1)pdm09 seroincidence of 4% after the first 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-confirmed influenza 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-
flect true seroconversion rates by HI.
Table 1. Influenza 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 Influenza Pandemic Among HIV-Infected and HIV-Uninfected
Men Who Have Sex With Men: Bangkok, Thailand, 2009–2011
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, 2010–July 31, 2010.
b
Time period after the third wave of the pandemic: January 1, 2011–March 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.
4•OFID •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 influenza virus infection, HIV-infected persons
in these studies were not severely immunocompromised, mak-
ing it difficult 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 influenza infection due to B-cell
dysfunction [17], thus accounting for the lack of differences in
susceptibility to influenza 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 influenza infection. Prior stud-
ies have demonstrated that HIV infection confers an increased
risk for severe influenza infection, supporting the importance of
targeted influenza vaccination among persons infected with
HIV [18].
Several points should be considered when interpreting our
findings. 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 find-
ings may suggest that Thai adults had relatively high levels of
preexisting cross-reactive antibody to A(H1N1)pdm09 from
prior infection with other influenza viruses [19]. However, de-
tection of cross-reactive antibodies to previously circulating in-
fluenza strains by MN is unlikely to have impacted our results
because we defined 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 reflect 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 first 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 influenza 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 influenza virus and to seasonal influenza viruses in ge-
neral. Given that persons infected with HIV are at risk for more
complicated illness once infected with influenza, these individ-
uals should continue to be prioritized for influenza vaccination
during seasonal influenza 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 findings 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 conflicts of interest. All authors: No reported conflicts.
All authors have submitted the ICMJE Form for Disclosure of Potential
Conflicts of Interest.
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