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,

Atlanta, GA 30329. E-mail: ahaynes1@cdc.gov

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. Defi ning

periods of elevated human metapneumovirus

circulation may guide virus detection and clinical

management, aiding in identifying illness and

outbreaks.

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HAYNES et al

First identified in 2001, 1 human

metapneumovirus (HMPV) is a

cause of both upper and lower

respiratory tract infections, including

bronchiolitis and pneumonia,

particularly among young children

(<5 years), the elderly, and

immunocompromised patients.2–5

Infection with HMPV has been

associated with an estimated 20 000

U.S. hospitalizations annually among

children aged <5 years.6 However,

the infrequent testing and low index

of suspicion associated with HMPV

may have limited the assessment

of temporal trends in HMPV

circulation. Also, many studies have

demonstrated that HMPV causes a

respiratory tract infection clinically

indistinguishable from infections

caused by respiratory syncytial virus

(RSV) and influenza.1–5 In contrast,

the specific prevention options and

some populations severely affected

vary for HMPV, RSV, and influenza.7

Currently there is no vaccine for

HMPV. Thus, describing HMPV

circulation in the United States in the

context of RSV and influenza may

help clinicians to prioritize diagnostic

testing, identify an etiologic agent,

manage patients clinically, and

choose appropriate prevention

strategies.

Many studies have demonstrated a

winter-to-spring circulation period

for HMPV in temperate climates, 8–10

but determination of national HMPV

trends and comparison of HMPV

seasonality to RSV and influenza

in multiple sites throughout the

United States have not yet been

done. A study conducted in 3 U.S.

sites identified HMPV circulation in

winter and spring months;6 however,

it remains unclear if this pattern

reflects trends in national HMPV

circulation. The increased availability

and use of molecular diagnostic

assays to detect respiratory viruses11

in recent years has highlighted

several HMPV-associated outbreaks

throughout the United States12 and

has enhanced the opportunity to

evaluate national trends in HMPV

circulation.

In the United States, surveillance

for several respiratory viruses is

conducted annually through the

National Respiratory and Enteric

Virus Surveillance System (NREVSS).

In this study, we describe national

HMPV circulation patterns and

compare with patterns of RSV and

influenza activity reported to NREVSS

during 6 seasons from 2008 to 2014.

METHODS

NREVSS is a passive surveillance

network established in 1984 that

collects specimen test results

for several respiratory viruses,

including HMPV, RSV, and influenza.

Approximately 300 clinical and

public health laboratories in the

United States report ≥1 specimen

test result on average for 44 weeks

in a surveillance year.13 Laboratories

report weekly aggregates of the

number of tests performed and

positive detections by antigen

detection, polymerase chain reaction

(PCR), and viral isolation. The type of

assay reported can vary depending

on the respiratory virus and year.

For RSV, we analyzed antigen

detection reports; for influenza,

we analyzed PCR reports; and for

HMPV, we analyzed both antigen

detection and PCR reports. The

NREVSS surveillance year is defined

as July of the starting year through

the end of the following June to

capture the typical national onset

and offset of several respiratory

viruses. Surveillance for RSV and

influenza through NREVSS is well

established and ongoing since 1984

and 1989, respectively. The first

HMPV diagnostic test was reported

to NREVSS in July 2005, but reports

were insufficient for robust analysis

until 2008 to 2009, when test reports

to NREVSS exceeded 70 000.

Laboratories included in this analysis

were selected based on annual

duration and volume of reported

test results. For RSV analysis, we

included laboratories reporting

≥10 RSV antigen detection tests/

week annually and ≥1 RSV antigen

detection test for 30 of 52 weeks

of the NREVSS year; for influenza

analysis, we included laboratories

reporting influenza by PCR to

the World Health Organization

collaborating laboratories;14 and

for HMPV analysis, we included

laboratories reporting ≥1 HMPV PCR

or antigen detection test for 36 of 52

weeks of the NREVSS year. These are

standard laboratory inclusion criteria

for RSV and influenza; no standard

inclusion criteria exist for HMPV.

For each virus, we calculated the

weekly proportion-positive. To

define the season for RSV13 and

influenza, 14 we used the widely

accepted 10% weekly proportion-

positive threshold. Specifically,

the RSV or influenza seasons were

defined as the first of 2 consecutive

weeks when the proportion of

positive weekly aggregates exceeded

10% positivity, and the season

offset, as the last of 2 consecutive

weeks when the proportion of

weekly aggregates exceeded 10%

positivity. To define the season for

HMPV, we selected a 3% weekly

proportion-positive threshold. We

defined the HMPV season onset

as the first of 2 consecutive weeks

when the proportion of positive

weekly aggregates exceeded 3%

positivity, and the season offset,

as the last of 2 consecutive weeks

when the proportion of weekly

aggregates exceeded 3% positivity.

At a threshold of 3%, 84% to 94%

of HMPV detections by antigen

detection tests were captured

each year, and 80% to 92% of

HMPV detections by PCR tests

were captured. For each virus, we

calculated the onset, offset, peak,

and duration (onset to offset) for

each individual season and the

median for the 6 seasons. A 4-season

median rather than a 6-season

median was calculated for influenza;

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PEDIATRICS Volume 137 , number 5 , May 2016

2 seasons (2008 to 2009, 2009 to

2010) were excluded because of the

unprecedented occurrence of the

H1N1 pandemic. An early season was

defined as a season with an earlier

onset than the 6-season median and

higher peak proportion-positive

than the 6-season median, and a late

season was defined as a later onset

than the 6-season median and lower

peak proportion-positive than the

6-season median.

RESULTS

Among all laboratories reporting

HMPV tests results to NREVSS from

July 2008 to June 2014, 1 065 742

HMPV test results were reported

and 38 160 (3.6%) were positive

(25 409 [3.9%] by PCR; 12 751

[3.0%] by antigen detection). Among

consistently reporting laboratories

included in our analysis, 945 836

tests were reported from July 2008

to June 2014, and 33 583 (3.6%)

were positive (21 972 [3.9%] by PCR,

11 611 [3.1%] by antigen detection)

for HMPV, 1 839 877 tests were

reported and 281 581 (15.3%) were

positive for RSV, and 2 206 654 tests

were reported (including specimens

from the H1N1 influenza pandemic)

and 401 342 (18.2%) were positive

for influenza. During the study

period, laboratories consistently

reporting HMPV comprised general

hospitals (60.3%), children’s

hospitals/facilities (28.9%), public

health facilities (9.6%), and reference

laboratories (1.2%). The number of

laboratories reporting HMPV tests

increased from 21 laboratories

representing 16 states in 2008 to

2009 to 60 laboratories representing

30 states in 2013 to 2014 (Table 1,

Fig 1). The number of HMPV tests

remained relatively constant over

the 6 surveillance years, but the

most prevalent diagnostic method

reported fluctuated from year to

year. In 2008 to 2009 and 2009 to

2010, 77% and 52%, respectively,

of HMPV diagnostic tests reported

were antigen detection; however,

from 4 seasons that spanned 2010 to

2014, 52% to 85% of diagnostic tests

reported were PCR. Similarly, the

number of laboratories consistently

reporting HMPV by antigen detection

decreased from the 2008 to 2009 to

2013 to 2014 season (median 21,

range 15 to 25), and the number

of laboratories reporting by PCR

increased from the 2008 to 2009 to

the 2013 to 2014 season (median 34,

range 9 to 49) (Table 1). Reporting

both test methods for HMPV by

laboratories was infrequent but

increased from 3 in 2008 to 2009 to 9

in 2013 to 2014.

The weekly proportion of specimens

positive by antigen detection or PCR

methods for HMPV show definitive

seasonal patterns each year (Fig 2A).

The weekly proportion of positive

HMPV tests ranged from a low of

<1% between July and November to

a maximum of 6% to 16% between

March and April. We observed a

slight biennial pattern with early

and late seasons for HMPV based on

the median weekly proportion-PCR

positive tests with early (NREVSS

surveillance years: 2009 to 2010,

2011 to 2012, and 2013 to 2014)

and late (NREVSS surveillance years:

2008 to 2009, 2010 to 2011, and

2012 to 2013) seasons (Fig 2B).

Nationally, the HMPV 6-season

median onset occurred in early

January (week 1), and individual

season onsets occurred from late

November to late February within

5 weeks of the 6-season median

3

TABLE 1 HMPV Diagnostic Tests Reported to NREVSS by Test Type and Year, United States, 2008 to 2014

NREVSS Year Antigen Detection PCR Totala

Laboratories

Reporting, n

States

Represented, n

Tests, n (%) Laboratories

Reporting, n

States

Represented, n

Tests, n (%) Laboratories

Reporting, n

States

Represented, n

2008 to 2009 15 14 69 698 (77) 9 8 20 353 (23) 21 16

2009 to 2010 20 17 83 033 (52) 20 12 77 342 (48) 33 21

2010 to 2011 21 17 76 710 (48) 32 17 83 155 (52) 46 25

2011 to 2012 25 19 59 935 (42) 35 18 83 241 (58) 53 28

2012 to 2013 24 18 60 573 (30) 43 21 141 709 (70) 62 31

2013 to 2014 20 15 28 881 (15) 49 28 161 206 (85) 60 30

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.

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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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HAYNES et al

participating laboratories can differ

from season to season and may

report different respiratory viruses;

(2) HMPV test reporting is relatively

new and does not garner the same

test reporting volume or regional

representation as more established

respiratory viruses, such as RSV; (3)

patient age and specific specimen

information are not collected; and

(4) duplication is a possibility if

antigen detection and PCR testing

are performed and reported on the

same specimen or if >1 specimen is

reported from a patient during the

same illness episode. Because HMPV

is a recently recognized respiratory

virus, health professionals may not

routinely consider or test for HMPV.

Finally, we selected a low positivity

threshold to define HMPV seasonality

because fewer detections were

positive for HMPV compared with

other respiratory viruses monitored

by NREVSS.

CONCLUSIONS

In the Unites States, HMPV circulates

in distinct annual seasons with

biennial patterns of early and late

seasons. Our findings suggest that

RSV onset occurs the earliest during

the fall/winter respiratory virus

season, followed by influenza and

then HMPV. To distinguish HMPV

from other cocirculating viruses,

health professionals should consider

HMPV testing during the respiratory

season, especially when HMPV is the

predominant virus circulating.

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6

ABBREVIATIONS

HMPV:  human metapneumovirus

NREVSS:  National Respiratory

and Enteric Virus

Surveillance System

PCR:  polymerase chain reaction

RSV:  respiratory syncytial virus

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2016 by the American Academy of Pediatrics

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

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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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