ARTICLE PEDIATRICS Volume 137, number 5, May 2016:e20152927 Human Metapneumovirus Circulation in the United States, 2008 to 2014 Amber K. Haynes, MPH, a Ashley L. Fowlkes, MPH, b Eileen Schneider, MD, a Jeffry D. Mutuc, MPH, a Gregory L. Armstrong, MD, c Susan I. Gerber, MD a abstract BACKGROUND: Human metapneumovirus (HMPV) infection causes respiratory illness, including bronchiolitis and pneumonia. However, national HMPV seasonality, as it compares with respiratory syncytial virus (RSV) and influenza seasonality patterns, has not been well described. METHODS: Hospital and clinical laboratories reported weekly aggregates of specimens tested and positive detections for HMPV, RSV, and influenza to the National Respiratory and Enteric Virus Surveillance System from 2008 to 2014. A season was defined as consecutive weeks with ≥3% positivity for HMPV and ≥ 10% positivity for RSV and influenza during a surveillance year (June through July). For each virus, the season, onset, offset, duration, peak, and 6-season medians were calculated. RESULTS: Among consistently reporting laboratories, 33 583 (3.6%) specimens were positive for HMPV, 281 581 (15.3%) for RSV, and 401 342 (18.2%) for influenza. Annually, 6 distinct HMPV seasons occurred from 2008 to 2014, with onsets ranging from November to February and offsets from April to July. Based on the 6-season medians, RSV, influenza, and HMPV onsets occurred sequentially and season durations were similar at 21 to 22 weeks. HMPV demonstrated a unique biennial pattern of early and late seasonal onsets. RSV seasons (onset, offset, peak) were most consistent and occurred before HMPV seasons. There were no consistent patterns between HMPV and influenza circulations. CONCLUSIONS: HMPV circulation begins in winter and lasts until spring and demonstrates distinct seasons each year, with the onset beginning after that of RSV. HMPV, RSV, and influenza can circulate simultaneously during the respiratory season. Divisions of a Viral Diseases, and b Influenza, National Center for Immunization and Respiratory Diseases, and c Office of Advanced Molecular Detection, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia Ms Haynes helped conceptualize and design the study and drafted the initial manuscript; Mr Mutuc carried out preliminary analyses; Mr Mutuc and Dr Armstrong reviewed the manuscript; Ms Fowlkes served as influenza virus subject matter expert; Ms Fowlkes and Dr Schneider helped design the study; Ms Fowlkes and Drs Schneider and Gerber critically reviewed the manuscript; Dr Schneider served as human metapneumovirus subject matter expert; Dr Armstrong conceptualized the study analysis; Drs Armstrong and Gerber revised the manuscript; Dr Gerber guided the study concept and design; and all authors approved the final manuscript as submitted. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. DOI: 10.1542/peds.2015-2927 Accepted for publication Jan 27, 2016 Address correspondence to Amber K. Haynes, MPH, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, 1600 Clifton Rd, NE, MS A-34, Atlanta, GA 30329. E-mail: [email protected]To cite: Haynes AK, Fowlkes AL, Schneider E, et al. Human Metapneumovirus Circulation in the United States, 2008 to 2014. Pediatrics. 2016;137(5):e20152927 WHAT’S KNOWN ABOUT THIS SUBJECT: Human metapneumovirus is a respiratory virus that causes upper and lower respiratory infections. Clinical presentation, populations most severely impacted, and circulation patterns are similar to those of respiratory syncytial virus; however, national human metapneumovirus circulation has not been well described. WHAT THIS STUDY ADDS: This study describes national human metapneumovirus circulation using laboratory detections reported to a national surveillance system from 2008 to 2014. Defining periods of elevated human metapneumovirus circulation may guide virus detection and clinical management, aiding in identifying illness and outbreaks. by guest on January 19, 2021 www.aappublications.org/news Downloaded from
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ARTICLEPEDIATRICS Volume 137 , number 5 , May 2016 :e 20152927
Human Metapneumovirus Circulation in the United States, 2008 to 2014Amber K. Haynes, MPH, a Ashley L. Fowlkes, MPH, b Eileen Schneider, MD, a Jeffry D. Mutuc, MPH, a Gregory L. Armstrong, MD, c Susan I. Gerber, MDa
abstractBACKGROUND: Human metapneumovirus (HMPV) infection causes respiratory illness, including
bronchiolitis and pneumonia. However, national HMPV seasonality, as it compares with
respiratory syncytial virus (RSV) and influenza seasonality patterns, has not been well
described.
METHODS: Hospital and clinical laboratories reported weekly aggregates of specimens tested
and positive detections for HMPV, RSV, and influenza to the National Respiratory and
Enteric Virus Surveillance System from 2008 to 2014. A season was defined as consecutive
weeks with ≥3% positivity for HMPV and ≥10% positivity for RSV and influenza during
a surveillance year (June through July). For each virus, the season, onset, offset, duration,
peak, and 6-season medians were calculated.
RESULTS: Among consistently reporting laboratories, 33 583 (3.6%) specimens were positive
for HMPV, 281 581 (15.3%) for RSV, and 401 342 (18.2%) for influenza. Annually, 6 distinct
HMPV seasons occurred from 2008 to 2014, with onsets ranging from November to
February and offsets from April to July. Based on the 6-season medians, RSV, influenza,
and HMPV onsets occurred sequentially and season durations were similar at 21 to 22
weeks. HMPV demonstrated a unique biennial pattern of early and late seasonal onsets.
RSV seasons (onset, offset, peak) were most consistent and occurred before HMPV seasons.
There were no consistent patterns between HMPV and influenza circulations.
CONCLUSIONS: HMPV circulation begins in winter and lasts until spring and demonstrates
distinct seasons each year, with the onset beginning after that of RSV. HMPV, RSV, and
influenza can circulate simultaneously during the respiratory season.
Divisions of aViral Diseases, and bInfl uenza, National Center for Immunization and Respiratory Diseases, and cOffi ce of Advanced Molecular Detection, National Center for Emerging and Zoonotic Infectious Diseases,
Centers for Disease Control and Prevention, Atlanta, Georgia
Ms Haynes helped conceptualize and design the study and drafted the initial manuscript;
Mr Mutuc carried out preliminary analyses; Mr Mutuc and Dr Armstrong reviewed the
manuscript; Ms Fowlkes served as infl uenza virus subject matter expert; Ms Fowlkes and
Dr Schneider helped design the study; Ms Fowlkes and Drs Schneider and Gerber critically
reviewed the manuscript; Dr Schneider served as human metapneumovirus subject matter
expert; Dr Armstrong conceptualized the study analysis; Drs Armstrong and Gerber revised the
manuscript; Dr Gerber guided the study concept and design; and all authors approved the fi nal
manuscript as submitted.
The fi ndings and conclusions in this report are those of the authors and do not necessarily
represent the offi cial position of the Centers for Disease Control and Prevention.
DOI: 10.1542/peds.2015-2927
Accepted for publication Jan 27, 2016
Address correspondence to Amber K. Haynes, MPH, National Center for Immunization and
Respiratory Diseases, Centers for Disease Control and Prevention, 1600 Clifton Rd, NE, MS A-34,
A total of 945 836 test results were reported for HMPV (antigen detection, 378 830 [40%]; PCR, 567 006 [60%]).a Total includes those qualifying laboratories reporting HMPV test results by antigen detection, PCR, or both diagnostic test methods.
FIGURE 1Geographic distribution of states with laboratories consistently reporting HMPV diagnostic test results by test type, United States, 2008 to 2014. n = number of states with qualifying laboratories consistently reporting HMPV test results for the specifi ed NREVSS Year. Laboratories reporting HMPV test results by antigen detection, PCR, or both diagnostic methods.
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HAYNES et al
onset (Table 2). The HMPV 6-season
median offset occurred in mid-May
(week 20) ranging from late April
to early July within 7 weeks of
the individual season offsets. The
6-season median peak occurred in
late March (week 12) and ranged
from late February (week 7) to early
May (week 17) for individual season
peaks. The HMPV 6-season duration
was 21 weeks (individual season
duration range 19 to 25 weeks). Only
minor variations in the occurrence
of the HMPV season onset, peak, and
offset were observed between PCR
and antigen detection methods.
The RSV seasons were most
consistent, with very little change
in onset, offset, and peak, unlike
HMPV and influenza (Fig 3). The
HMPV season onset, offset, and
peak occurred after RSV for all 6
seasons. Year-to-year patterns in
the sequential occurrence of offset
and peak were similar among RSV
and HMPV, but not influenza (Table
2). The 6-season median onset for
RSV, influenza, and HMPV occurred
in sequential order (Table 2). The
first respiratory virus season median
onset to occur was RSV, which had
a 6-season median onset in early
November (individual season onset
range late October to late November).
The influenza 4-season median
onset occurred in early December,
4
FIGURE 2Human metapneumovirus reporting by diagnostic test type (A) and early and late seasons (B), United States, 2008 to 2014. *Three-week moving average (average of the previous, current, and following week proportion of positive tests for each testing method) of the median weekly proportion-PCR positive tests and antigen positive tests. †Early seasons: 2009 to 2010, 2011 to 2012, 2013 to 2014; late seasons: 2008 to 2009, 2010 to 2011, 2012 to 2013.
TABL
E 2
Sea
son
On
set,
Off
set,
Pea
k, a
nd
Du
rati
on f
or R
SV,
Infl
uen
za, a
and
HM
PV
for
Ind
ivid
ual
Sea
son
s an
d t
he
6-S
easo
n M
edia
n, U
nit
ed S
tate
s, 2
008
to 2
014
NR
EVS
S Y
ear
Mon
th O
nse
t O
ccu
rred
(M
MW
R W
eek)
Mon
th O
ffse
t O
ccu
rred
(M
MW
R W
eek)
Mon
th P
eak
Occ
urr
ed (
MM
WR
Wee
k)S
easo
n D
ura
tion
, Wee
ks
RS
VIn
fl u
enza
HM
PV
RS
VIn
fl u
enza
HM
PV
RS
VIn
fl u
enza
HM
PV
RS
VIn
fl u
enza
HM
PV
2008
to
2009
Nov
(44
)Ja
n (
02)
Jan
(02
)M
ar (
11)
Apr
(14)
May
(20
)Ja
n (
3)Fe
b (
6)M
ar (
12)
2013
19
2009
to
2010
Nov
(45
)Ap
r (1
7)D
ec (
52)
Mar
(12
)D
ec (
48)
May
(19
)Ja
n (
3)Ju
n (
24)
Feb
(9)
2032
20
2010
to
2011
Nov
(46
)N
ov (
47)
Jan
(04
)Ap
r (1
4)Ap
r (1
4)Ju
l (27
)Fe
b (
5)Fe
b (
5)M
ay (
17)
2120
24
2011
to
2012
Nov
(46
)Fe
b (
05)
Dec
(48
)Ap
r (1
4)Ju
n (
24)
Apr
(16)
Jan
(4)
Mar
(10
)Fe
b (
7)21
2021
2012
to
2013
Oct
(43
)N
ov (
45)
Feb
(07
)M
ar (
13)
Apr
(15)
Jul (
27)
Jan
(1)
Dec
(52
)Ap
r (1
4)23
2321
2013
to
2014
Nov
(45
)D
ec (
48)
Nov
(48
)M
ar (
13)
May
(20
)M
ay (
20)
Dec
(52
)D
ec (
52)
Mar
(12
)21
2525
6-S
easo
n M
edia
na
Nov
(45
)D
ec (
48)a
Jan
(01
)M
ar (
13)
May
(18
)aM
ay (
20)
Jan
(3)
Jan
(3)
aM
ar (
12)
21b
22a,
b21
b
a In
fl u
enza
6-s
easo
n m
edia
ns
excl
ud
e th
e 20
08 t
o 20
09 a
nd
200
9 to
201
0 se
ason
s b
ecau
se o
f th
e H
1N1
pan
dem
ic.
b T
he
6-se
ason
med
ian
for
sea
son
du
rati
on is
bas
ed o
n t
he
med
ian
of
the
seas
on d
ura
tion
for
th
e 6
seas
ons
(4 s
easo
ns
for
infl
uen
za)
and
not
th
e d
iffe
ren
ce o
f th
e 6-
seas
on m
edia
n f
or t
he
onse
t an
d o
ffse
t.
by guest on January 19, 2021www.aappublications.org/newsDownloaded from
PEDIATRICS Volume 137 , number 5 , May 2016
(individual season onset range
late November to early February).
The HMPV 6-season median onset
occurred in early January (individual
season onset range late November to
late February). The first respiratory
virus season offset to occur was RSV.
The 6-season median offset for RSV
occurred in late March (individual
season offset range mid-March to
early April), followed by influenza in
early May (individual season offset
range early April to early June) and
HMPV in mid-May (individual season
offset range late April to early July).
The 6-season median peak occurred
in the following sequential order:
RSV (late January, week 3), influenza
(late January, week 3), and HMPV
(late March, week 12). The 6-season
median onset and peak for HMPV
occurred 8 and 9 weeks, respectively,
after RSV and 5 and 9 weeks after
influenza, respectively (Table 2). The
6-season median duration for all 3
viruses were very similar at 21 to 22
weeks.
DISCUSSION
This is the first published summary
of HMPV national data from NREVSS
and demonstrates several unique
features. From 2008 to 2014, the
national HMPV data suggest that
HMPV seasons occur later than RSV
seasons, and based on the 6-season
median onset, the RSV season
occurred first, followed by influenza
and then HMPV. The unprecedented
H1N1 influenza pandemic that
affected the 2008 to 2009 and 2009
to 2010 seasons made comparison
during these seasons difficult
to interpret. In addition, HMPV
demonstrated a biennial pattern of
early and late seasons. There were
no distinct differences in HMPV
seasonality determined by antigen
detection and PCR, and PCR was the
most prevalent diagnostic method
used to identify HMPV in the last 4
years of analysis.
HMPV season durations occurred
between November and July
(6-season median 21 weeks). Weekly
HMPV positivity fluctuated between
nearly zero and ≥6% every 12
months, showing a distinguishable
seasonal pattern. Similar to RSV
and influenza, HMPV seasons
occurred during winter and spring,
as previously described.8–10 The
weekly HMPV percent-positivity
in this analysis never reached zero
over the 6 years of surveillance,
confirming previous reports of low
but continuous HMPV circulation
beyond winter and spring.15 We also
observed a biennial pattern for HMPV
of alternating early and late season
from 2008 to 2014, which was not
seen for RSV or influenza.16, 17
The most prevalent HMPV diagnostic
method reported shifted from
antigen detection to PCR during 2008
to 2014. The shift toward increased
reporting of PCR tests likely reflects
changes in conventional diagnostic
testing among participating NREVSS
laboratories. Within any given season
during this time period, a 3% weekly
positivity measure captured ≥80%
of PCR HMPV detections reported
by qualifying institutions. The 3%
weekly proportion is comparatively
lower than the 10% positivity used to
indicate elevated influenza and RSV
circulations. However, as in other
studies, we determined that a smaller
proportion of diagnostic tests were
positive for HMPV compared with
other respiratory pathogens.18–21
The data analyzed were not robust
enough to assess regional trends in
HMPV circulation.
The cocirculation analysis suggest
that HMPV, RSV, and influenza
cocirculate, as previously described
by Esper et al.15 Although the
circulations of influenza, RSV, and
HMPV overlap, the populations
susceptible to severe infection and
the management of these infections
differ.22–24
Therefore, clinicians can use
surveillance data, such as NREVSS,
to help identify HMPV seasonality
and help prioritize HMPV testing in
patients with respiratory symptoms.
As laboratory recruitment into
NREVSS and PCR use continue to
increase throughout the United States,
future NREVSS data should be able to
more reliably allow for more detailed
analyses, including regional HMPV
trends and outbreak occurrence,
similar to those for RSV and influenza.
Our study had several limitations.
Our findings are based on NREVSS,
which is a passive and voluntary
surveillance system in which (1)
5
FIGURE 3Onset, offset, peak, and duration by season and 6-season median for HMPV, RSV, and infl uenza, United States, 2008 to 2014. 2008 to 2009 and 2009 to 2010 infl uenza seasons not included in the 4-season median because of H1N1 pandemic.
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FINANCIAL DISCLOSURE: The authors have indicated they have no fi nancial relationships relevant to this article to disclose.
FUNDING: Supported by the Centers for Disease Control and Prevention, National Center for Immunization and Respiratory Diseases, Division of Viral Diseases
and Infl uenza.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential confl icts of interest to disclose.
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PEDIATRICS Volume 137 , number 5 , May 2016
2003-04 season, and composition of the
2004-05 infl uenza vaccine. MMWR Morb
Mortal Wkly Rep. 2004;53(25):547–552
15. Esper F, Martinello RA, Boucher
D, et al. A 1-year experience with
human metapneumovirus in
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16. Reiche J, Jacobsen S, Neubauer K,
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17. Aberle SW, Aberle JH, Sandhofer
MJ, Pracher E, Popow-Kraupp T.
Biennial spring activity of human
metapneumovirus in Austria. Pediatr
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18. Boivin G, De Serres G, Côté S, et al.
Human metapneumovirus infections in
hospitalized children. Emerg Infect Dis.
2003;9(6):634–640
19. Mullins JA, Lamonte AC, Bresee JS,
Anderson LJ. Substantial variability in
community respiratory syncytial virus
season timing. Pediatr Infect Dis J.
2003;22(10):857–862
20. Williams JV, Wang CK, Yang CF,
et al. The role of human
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respiratory tract infections in
children: a 20-year experience. J
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21. Chano F, Rousseau C, Laferrière C,
Couillard M, Charest H. Epidemiological
survey of human metapneumovirus
infection in a large pediatric tertiary
care center. J Clin Microbiol.
2005;43(11):5520–5525
22. Glezen WP, Taber LH, Frank AL,
Kasel JA. Risk of primary infection
and reinfection with respiratory
syncytial virus. Am J Dis Child.
1986;140(6):543–546
23. Centers for Disease Control and
Prevention. Prevention and control
of seasonal infl uenza with vaccines:
Recommendations of the advisory
committee on immunization
practices—United States, 2013-
2014. MMWR Morb Mortal Wkly Rep.
2013;62(RR07):1–43
24. Bastien N, Ward D, Van Caeseele P, et
al. Human metapneumovirus infection
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DOI: 10.1542/peds.2015-2927 originally published online April 4, 2016; 2016;137;Pediatrics
Armstrong and Susan I. GerberAmber K. Haynes, Ashley L. Fowlkes, Eileen Schneider, Jeffry D. Mutuc, Gregory L.
Human Metapneumovirus Circulation in the United States, 2008 to 2014
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