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Original Research

Novel influenza A(H1N1) outbreak among French armed forcesin 2009: Results of Military Influenza Surveillance System

A. Mayet a,*, S. Duron a, P. Nivoix b, R. Haus-Cheymol a, C. Ligier a, K. Gache a, A. Dia b,G. Manet a, C. Verret a, V. Pommier de Santi b, C. Bigaillon c, C. Martinaud d, M. Piarroux b,N. Faure b, C. Hupin b, C. Decam b, H. Chaudet b, J.B. Meynard a, E. Nicand e, X. Deparis b,R. Migliani a

aDepartment of Epidemiology and Public Health, Northern Sector, Val-de-Grace School of Military Medicine, Paris, FrancebDepartment of Epidemiology and Public Health, Southern Sector, Institute of Tropical Medicine, Military Health Department, Marseille,

FrancecDepartment of Biology, Begin Military Teaching Hospital, Saint Mande, FrancedDepartment of Biology, Percy Military Teaching Hospital, Clamart, FranceeDepartment of Biology, Val-de-Grace Military Teaching Hospital, Paris, France

a r t i c l e i n f o

Article history:

Received 23 June 2010

Received in revised form

7 December 2010

Accepted 25 April 2011

Available online 20 July 2011

Keywords:

Armed forces

A(H1N1)pdm09 influenza

Pandemic

* Corresponding author. Departement d’Epid94160 Saint Mande, France. Tel.: þ33 1 43 98

E-mail address: aurelie_marie@hotmail.fr0033-3506/$ e see front matter ª 2011 The Rdoi:10.1016/j.puhe.2011.04.005

s u m m a r y

Objectives: An outbreak of novel A(H1N1) virus influenza, detected in Mexico in April 2009,

spread worldwide in 9 weeks. The aim of this paper is to present the monitoring results of

this influenza outbreak among French armed forces.

Study design: The period of monitoring by the Military Influenza Surveillance System (MISS)

was 9 months, from May 2009 to April 2010.

Methods: The main monitored events were acute respiratory infection (ARI), defined by oral

temperature �38.5 �C and cough, and laboratory-confirmed influenza. Weekly incidence

rates were calculated by relating cases to the number of servicepersons monitored.

Results: In continental France, the incidence of ARI increased from September 2009, with

a weekly maxima of 401 cases per 100,000 in early December 2009 according to MISS.

Estimations of the incidence of consultations which could be related to novel A(H1N1)

influenza ranged from 48 to 57 cases per 100,000.

Conclusions: The trends observed by MISS are compatible with French national estimations.

The incidence of consultations which could be related to A(H1N1) influenza at the peak of

the epidemic (194 cases per 100,000) was much lower than the national estimate (1321

cases per 100,000). This may be due to servicepersons who consulted in civilian facilities

and were not monitored. Other explanations are the healthy worker effect and the younger

age of the military population.

ª 2011 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.

emiologie et de Sante Publique Nord, Ecole du Val-de-Grace, Ilot Begin, 69 avenue de Paris,49 96; fax: þ33 1 43 98 54 33.(A. Mayet).oyal Society for Public Health. Published by Elsevier Ltd. All rights reserved.

p u b l i c h e a l t h 1 2 5 ( 2 0 1 1 ) 4 9 4e5 0 0 495

Introduction

Influenza is a seasonal disease that is monitored interna-

tionally due to the high mutation rate of the influenza

viruses.1e3 Since 1997, the French military health service has

monitored the spread of influenza among military personnel

via the Military Influenza Surveillance System (MISS).4 The

MISS is a seasonal monitoring system activated each year in

autumn and winter, which is fully integrated with the French

national influenza monitoring network.4,5 The primary aim of

the MISS is rapid detection of the occurrence of influenza

outbreaks, and detection of any variance in circulating viral

strains. Influenza may disseminate rapidly within pop-

ulations who live in confined settings, causing significant

morbidity and disrupting daily activity. This could have

deleterious consequences among military personnel.6,7

Unexpectedly, a swine-origin influenza epidemic occurred

in North America (Mexico and the USA) toward the end of the

2008e2009 influenza season. The epidemic-related virus, iso-

lated on 21 April 2009 in two patients living in California,

appeared to be a novel swine-origin influenza virus. This virus

expressed an HA gene derived from the 1919 swine influenza

virus and other genes from human, avian and Eurasian swine

influenza viruses.8e11

On 24 April 2009, the World Health Organization (WHO)

issued a safety alert. The same type of A(H1N1) viral strainwas

discovered in Mexico, where the first case was retrospectively

dated on 17March 2009, and in Canada. Shortly thereafter, the

influenza virus began to spread worldwide. In France, the first

two cases were identified at the end of April 2009, and clusters

of cases were rapidly observed in the general population

throughout the country. WHO raised the influenza pandemic

alert level to 5 in April 2009, and subsequently to 6 in June

2009.12e14 On 27 November 2009, WHO reported more than

622,482 confirmed cases throughout the world, including 7826

deaths. Intensification of the outbreak occurred in continental

Europe in November 2009.15 France reported 188 serious cases,

including 86 deaths, since the beginning of the outbreak.16

Faced with this pandemic, the MISS was re-activated on 4

May 2009.17 The aim of this report is to present themonitoring

results of the novel A(H1N1) influenza among French military

forces from May 2009 to April 2010.

Table 1 e Primers and probes used to detect A(H1N1) 2009influenza virus by real-time polymerase chain reaction.

Targeted gene Name Sequences

A Influenza M GRAM/7Fw CTT CTA ACC GAG GTC

GAA ACG TA

GGT GAC AGG ATT GGT CTT

GTC TTT A

Fam-TCA GGC CCC CTC AAA

GCC GAG-BHQ-1

H1sw GRswH1-349Fw GAG CTA AGA GAG CAA TTG A

GTA GAT GGA TGG TGA ATG

Fam-TTG CTG AGC TTT GGG

TAT GA -BHQ-1

GAPDH GAPDH-6Fw GAA GGT GAA GGT CGG AGT

GAA GAT GGT GAT GGG ATT TC

Fam-CAA GCT TCC CGT TCT

CAG CC -BHQ-1

GAPDH, glyceraldehyde-3-phosphate dehydrogenase.

Methods

TheMISS is composed of volunteermedical services belonging

to 30 sentinel units, selected from the 320 existing military

units in continental France, based on their geographical

location to ensure optimal coverage of the territory. In 2009,

these sentinel units included 42,515military personnel, which

accounted for 14% of the military workforce in continental

France (42,515/309,233). This population only includesmilitary

personnel in active service, and does not include any depen-

dents, such as families living with service members. Two

health events are surveyedweekly: acute respiratory infection

(ARI), defined as acute catarrh of the aero respiratory system,

with oral temperature �38.5 �C and cough; and confirmed

influenza on nasopharyngeal swab [rapid diagnostic test or

one step real-time reverse transcriptase polymerase chain

reaction (rRT-PCR) or culture].

Some indirect indicators are also surveyed on a weekly

basis:

� number of consultations performed by the military medical

centre;

� number of personnel on sick leave (all causes) for <15 days,

including ARI, prescribed by the military medical centre;

and

� number of nasopharyngeal swabs taken for influenza

research.

MISS physicians take nasopharyngeal samples from

patients with ARI as follows: the first patient of the week is

sampled, and more than one patient is sampled if there is

a cluster of cases or unexpected symptoms. Research on

influenza viruses is being conducted in seven laboratories in

military teaching hospitals.

Once the novel A(H1N1) influenza virus was detected in

France, weekly epidemiological monitoring by the MISS was

re-activated on 4 May 2009, 5 months prior to the theoretical

start of the 2009e2010 influenza season. The laboratory-based

monitoring was only re-activated in July due to insufficient

information on the pathogenicity of this virus. The French

health authorities decided to give permission for a few

selective and specialized laboratories to test the samples until

22 June 2009. Then, rRT-PCR was performed systematically by

military teaching hospital laboratories for any viral detec-

tion,18 using the test recommended by the French Influenza

Reference National Centre, based on the protocol of the US

Centers for Disease Control and Prevention.19 Each sample

was tested by three rRT-PCR systems: (1) an rRT-PCR assay

targeting all influenza A viruses; (2) an rRT-PCR assay specific

for the novel A(H1N1) variant; and (3) an rRT-PCR assay tar-

geting human glyceraldehyde-3-phosphate dehydrogenase as

the extraction control gene. The primers and probes were

developed and provided by the French National Reference

Centre for Influenza Viruses (Table 1). Positive samples

p u b l i c h e a l t h 1 2 5 ( 2 0 1 1 ) 4 9 4e5 0 0496

detected between June and October were sent to the French

National Reference Centre for Influenza Viruses, which also

tested the resistance of the strains to neuraminidase inhibi-

tors (mutation at position 274H of neuraminidase glycopro-

tein) on samples received from hospitalized cases or those

who had developed an infection despite prior antiviral

treatment.

The ARI epidemic threshold was computed using the

current/past graphmethod, which compares the events of the

previous 4 weeks with a historical mean calculated using

the corresponding 4-week period over the previous 4 years.20

The incidence rates were calculated by dividing the weekly

number of cases (ARI and sick leave) by the number ofmilitary

personnel monitored per week (incidence rates in person-

weeks). The incidence of consultations which could be

attributed to novel A(H1N1) virus was estimated by multi-

plying the proportion of positive results among the samples

taken by the ARI incidence rate. The confidence intervals (CI)

of these estimations were calculated on the basis of the

Poisson distribution. Finally, the incidence rate for the week

when the epidemicwas at its peakwas comparedwith civilian

data after direct standardization of the French national pop-

ulation distribution for age. For three age strata (<20, 20e49,

�50 years), the number of forecasted cases was computed by

multiplying the incidence rate observed in the MISS by the

number of subjects in the French general population.

Results

During the study period (from Week 19 2009 to Week 5 2010),

the mean population monitored each week was 43,067 mili-

tary personnel. The ARI epidemic threshold was exceeded

from Weeks 33e35 2009 and from Weeks 44e53 2009. As

shown in Fig. 1, the first increase in the incidence of ARI began

in mid-August 2009 (Week 33 2009). A secondary increase,

higher than the previous increase, was observed from mid-

October (Week 42 2009), reaching a peak of 401 cases per

100,000 person-weeks, until the beginning of December (Week

49 2009) before decreasing. As shown in Fig. 2, the proportion

of cases of ARI among consultations was approximately 0.5%

in July, and increased steadily in August to reach 2.0%

between September and October 2009, and 5.0% between

November (Week 45) and December (Week 50) 2009.

Similarly, the first increase in the incidence of sick leave

was observed in September (Week 3 2009), peaking at 600

cases of sick leave per 100,000 person-weeks at the beginning

of October (Week 41 2009) (Fig. 1). The second peak, higher

than the first (900 cases of sick leave per 100,000 person-

weeks), occurred simultaneously with the peak in ARI (Week

49 2009), following an important increase at the beginning of

November (Week 45 2009).

The first case of influenza A(H1N1) 2009 in the French

armed forces was confirmed on 23 June 2009. Between May

2009 (Week 19 2009) and January 2010 (Week 5 2010), 649

nasopharyngeal swabs were tested. Of these, 239 (37%) were

found to be positive for novel A(H1N1) 2009 virus, nine were

positive for other A subtype viruses, and onewas positive for B

subtype virus. The positivity rate during the epidemic period

(506 swabs analyzed from Week 44 to Week 53 2009) was 58%.

A(H1N1) 2009 virus represented 96% of influenza viruses iso-

lated by the MISS. No resistance to neuraminidase inhibitors

was detected among these positive samples. None of the

confirmed cases were hospitalized and no deaths from influ-

enza were reported.

During the ARI epidemic period, the incidence of consul-

tations which could be attributed to A(H1N1) 2009 influenza

was estimated to be 56 (95% CI 51e60) cases per 100,000

person-weeks (Table 2 and Fig. 1). The incidence increased

significantly from the end of October 2009 (Week 44 2009),

peaking in Week 49 2009 [194 (95% CI 182e203) per 100,000

person-weeks]. As shown in Table 3, the highest incidence

rates were observed among subjects aged �50 years (484.3

cases per 100,000 person-weeks) and <20 (329.7 cases per

100,000 person-weeks) at Week 49 2009. After standardization

for age, the incidence rate in French military personnel at the

peak of the epidemic was estimated to be 287.8 cases per

100,000 person-weeks.

Discussion

The A(H1N1) 2009 influenza outbreak among French armed

forces was characterized in continental France by a high

increase in incidence toward the end of October 2009, which

peaked in November 2009. These trends were similar to the

estimates for the French civilian population.21 The increase in

the incidence of sick leave appeared to be correlated to the

wave of the epidemic, underlining the usefulness and rele-

vance of surveillance of indirect indicators, which have good

sensitivity and are relatively simple to collect.

The ARI epidemic threshold exceeded for 3 weeks in

August 2009, which coincided with the occurrence of some

clusters of cases among MISS units, and from Weeks 44e53

2009, corresponding with the peak of the epidemic. The fact

that the threshold was not exceeded from September to the

beginning of October 2009 reflects the relatively high ARI

incidence rates observed by the MISS during the correspond-

ing periods of previous years. This is a likely consequence of

the usual circulation of respiratory syncytial virus, respon-

sible for ARI epidemics in September.

Estimates of the incidence of consultations which could be

attributed to novel A(H1N1) virus among the French armed

forces at the peak of the epidemic ranged from182 to 203 cases

per 100,000 person-weeks, and were much lower than the

estimate for the French civilian population (approximately

850,000 consultations between Weeks 48 and 49 2009, or 1321

per 100,000 person-weeks).22,23 Such a difference could be

explained by the specific age range (20e49 years) which

represents 92% of the military population, while only 53% of

the whole French population belongs to this age group (Table

3).23 Also, young people, who are not represented in the

military population, were affected by the influenza pandemic.

For instance, the Canadian surveillance system reported that

48% of confirmed cases at the peak of the epidemic were aged

<18 years (vs 51% for 18e64-year-old subjects and 1% for

subjects aged �64 years).24 However, standardization for the

French civilian population only resulted in an incidence rate

of 287.8 per 100,000 person-weeks at the peak of the epidemic,

which indicates that the age structure of the military

0

50

100

150

200

250

300

350

400

450

500

550

600

19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 1 2 3 4 5

week

AR

I an

d A

(H

1N

1) in

flu

en

za In

cid

en

ce rates (p

.100,000)

0

100

200

300

400

500

600

700

800

900

Sick leave in

cid

en

ce rate (p

.100,000

)

ARIA(H1N1) linked consultationsSick leaves

ARI epidemic period

Fig. 1 e Incidence of acute respiratory infection (ARI), sick leave lasting <15 days and consultations due to A(H1N1) 2009

influenza: Week 19 2009 to Week 5 2010.

p u b l i c h e a l t h 1 2 5 ( 2 0 1 1 ) 4 9 4e5 0 0 497

population only partially explains the low incidence. Consul-

tations with military physicians are not compulsory, and

some military personnel may have consulted civilian physi-

cians during the outbreak, which could explain the low inci-

dence of ARI among military personnel. Moreover, military

personnel are enrolled according to specific health criteria,

and are consequently in better health than the civilian pop-

ulation as a whole, particularly due to the absence of pathol-

ogies that could increase the risk of influenza (e.g. unstable

asthma, morbid obesity, chronic immunological deficiency,

0

20

40

60

80

100

120

140

160

180

19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39

week

AR

I in

cid

en

ce

ARI

Fig. 2 e Incidence of acute respiratory infection (ARI) and propo

Week 5 2010.

etc.). Finally, vaccination coverage against novel A(H1N1)

influenza was slightly better among military personnel

(14.5%)26 than among civilians (7.9%).25

Since 1999, military personnel have been vaccinated every

3 years; the aim of this is not to protect individuals, but to

achieve collective immunity by protecting part of the work-

force.27 In consideration of the pandemic situation, vaccina-

tion with the 2009e2010 seasonal vaccine was recommended

for all military personnel in September 2009, just before the

programme of vaccination against pandemic influenza.

40 41 42 43 44 45 46 47 48 49 50 51 52 53 1 2 3 40%

1%

2%

3%

4%

5%

6%

Pro

po

rtio

n o

f A

RI a

mo

ng

co

nsu

latio

ns

% ARI / consultations

rtion of cases of ARI among consulations: Week 19 2009 to

Table 2 e Incidence (per 100,000 person-weeks) of consultations due to A(H1N1) 2009 influenza among French militarypersonnel: Week 19 2009 to Week 5 2010.

Week 2005e2009Baseline incidence

of ARIa

2009e2010Incidence of ARI

2009e2010 Numberof samples

2009e2010Positive samples

Positivity rate (%) Incidence of A(H1N1)2009 influenza

19 48.3 11.2 0 0 0 0.0

20 51.3 17.6 0 0 0 0.0

21 40.6 2.2 0 0 0 0.0

22 41.2 11.0 0 0 0 0.0

23 48.9 13.0 0 0 0 0.0

24 51.3 37.5 0 0 0 0.0

25 38.2 19.9 3 0 0 0.0

26 33.4 13.6 0 0 0 0.0

27 20.9 9.2 0 0 0 0.0

28 23.9 7.0 0 0 0 0.0

29 19.1 7.0 2 0 0 0.0

30 9.0 2.5 2 0 0 0.0

31 10.1 5.5 0 0 0 0.0

32 14.9 16.3 4 0 0 0.0

33 10.7 21.0 5 1 20 4.2

34 13.7 37.3 17 1 6 2.2

35 28.0 76.8 25 4 16 12.3

36 37.0 39.6 15 1 7 2.6

37 51.3 65.2 18 13 72 46.9

38 81.7 81.5 26 7 27 22.0

39 106.2 88.5 44 9 21 18.1

40 140.0 79.2 24 1 4 3.3

41 176.5 125.7 26 1 4 2.2

42 135.9 72.2 12 3 25 18.1

43 145.9 99.4 15 5 33 33.1

44 91.8 108.4 25 20 80 86.8

45 128.2 207.8 57 29 51 105.7

46 114.1 223.7 34 24 71 157.9

47 193.5 311.8 56 30 54 167.0

48 146.5 321.5 58 25 43 138.6

49 157.6 401.9 62 30 48 194.4

50 139.4 306.6 34 15 44 135.3

51 132.4 242.1 15 8 53 129.1

52 17.6 100.0 3 3 100 100.0

53 17.6 60.0 4 1 25 15.0

1 118.2 38.7 12 2 17 6.6

2 102.9 65.9 14 5 36 23.7

3 182.4 64.3 4 2 50 32.1

4 214.1 64.2 5 0 0 0.0

5 319.4 49.4 3 0 0 0.0

Total 168.9 506 208 38 56.2

ARI, acute respiratory infection.

Bold values indicate period when the ARI epidemic threshold was exceeded.

a Mean incidence for previous four influenza seasons.

p u b l i c h e a l t h 1 2 5 ( 2 0 1 1 ) 4 9 4e5 0 0498

Among cases of ARI documented with a nasopharyngeal

swab, the proportion of people vaccinated with the 2009e

2010 seasonal vaccine was the same (approximately 16%) in

those testing positive and negative for novel A(H1N1) virus

(A. Mayet et al., unpublished data). Thus, individual history

of seasonal vaccination is not likely to explain the lower

susceptibility of military personnel to developing novel

A(H1N1) influenza.

Concerning the limitations of this study, estimates of the

incidence of consultations due to novel A(H1N1) virus were

inferred from the incidence of ARI using the proportion of

positive samples, while the proportion of sampled patients

among those with ARI is relatively low. In addition, incidence

rates were estimated from only 14% of the military workforce.

Thus, these estimations should be interpreted with caution.

This is illustrated by the marked variability in the positivity

rates,which induces variations in the estimated incidence rates

for influenza. This is a consequence of clusters of cases which

led toMISSphysicians taking numerous nasopharyngeal swabs

during the same week. However, these variations in incidence

are compensated for by the global trend in ARI, and the reli-

ability ofMISS results is likely due to the application of a quality

standard (physicians involved in this network undergo training

each year on monitoring and sampling schemes).

In conclusion, French armed forces re-activated the MISS

precociously in the A(H1N1) influenza pandemic. This

Table 3 e Incidence (per 100,000 person-weeks) of consultations due to A(H1N1) 2009 influenza among French militarypersonnel at the peak of the epidemic, and direct standardization with the French general population: Week 49 2009.

Age(years)

Servicepersons(MISS)a

Numberof casesof ARIb

Incidenceof ARI

(IR per 100,000)

% Positivesamples

EstimatedIR of

influenza(per 100,000)

French populationstructurec

Forecastedinfluenza casesd

StandardizedIRe

<20 849 (2%) 11 1318.6 25% 329.7 16,075,000 (25%) 52,993 e

20e49 38,644 (92%) 146 376.8 50% 188.4 34,722,000 (53%) 65,411 e

�50 2312 (6%) 11 484.3 100% 484.3 14,146,000 (22%) 68,516 e

Total 41,806 168 401.9 48% 194.4 64,943,000 186,920 287.8

MISS, Military Influenza Surveillance System; ARI, acute respiratory infection; IR, incidence rate.

a Estimated from data of the whole military workforce structure.

b Estimated from distribution of laboratory-confirmed cases of influenza.

c Data from French National Institute of Demographic Studies.

d In each age group, number of subjects in French population multiplied by estimated IR for influenza.

e Standardized IR ¼ (186,920/64,943,000) � 100,000.

p u b l i c h e a l t h 1 2 5 ( 2 0 1 1 ) 4 9 4e5 0 0 499

outbreak disrupted military activities in some units, which

were forced to cancel training, but had little impact on major

international operations, except some circumscribed

outbreaks among soldiers in Afghanistan and on few Navy

ships. Finally, the results of this surveillance were compatible

with the West European epidemic trends.

Ethical approval

French military epidemiological surveillance networks which

use anonymous data, including the MISS, were approved by

the ethical committee of the French military health service.

For this study, the data were extracted from weekly epide-

miological reports which did not contain nominative data.

Funding

None declared.

Competing interests

None declared.

Acknowledgments

The authors would like to thank all the military physicians,

the staff of the epidemiological and public health depart-

ments, and the biologists of the Frenchmilitary health service

who participated actively in the MISS by way of the quality of

their notifications and reports. The authors also thank

Dr. Remi Michel for his help.

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