Early Stages of
Alex Marchand-Austin, David J. Farrell, Frances
B. Jamieson, Nino Lombardi, Ernesto Lombos,
Sunita Narang, Holy Akwar, Donald E. Low, and
Jonathan B. Gubbay
Outbreaks of respiratory infection in institutions in On-
tario, Canada were studied from April 20 to June 12, 2009,
during the early stages of the emergance of infl uenza A
pandemic (H1N1) 2009. Despite widespread presence of
infl uenza in the general population, only 2 of 83 outbreaks
evaluated by molecular methods were associated with pan-
demic (H1N1) 2009.
ment for disease transmission (1). Patients in long-term
care facilities (LTCFs) for the elderly are more susceptible
to respiratory infections and have a higher risk for compli-
espiratory infection outbreaks in institutions housing
large numbers of residents create an ideal environ-
We reviewed respiratory infection outbreaks regis-
tered with the Public Health Laboratory (PHL), Ontario
Agency for Health Protection and Promotion dating back to
October 2007 (Table 1). Molecular detection methods were
used for a subset of outbreaks registered during October 1,
2008–April 19, 2009. After emergence of severe respira-
tory illness clusters in Mexico in early April, intensifi ed
tracking of respiratory infection outbreaks in Ontario was
undertaken. Consequently, more information was available
on outbreaks registered during the spring (April 20 to June
12, 2009); these data comprise the bulk of the study.
Respiratory infection outbreaks in LTCFs were de-
fi ned as any of the following: 2 cases of acute respiratory
tract illness, 1 of which was laboratory-confi rmed; 3 cases
of acute respiratory tract illness within 48 hours in a geo-
graphic area (e.g., unit, fl oor); and >2 units having a case of
acute respiratory illness within a 48-hour period. Infl uenza-
like-illness was defi ned as acute onset of respiratory illness
with fever and cough with >1 of the following: sore throat,
arthralgia, myalgia, or prostration.
From April 20 through June 12, 2009, a total of 112
respiratory infection outbreaks were registered. Molecular
testing was not used in 29 outbreaks (e.g., insuffi cient/in-
appropriate sample). Most of the remaining 83 outbreaks
submitted for molecular testing originated from LTCFs
(91%); hospitals (2%), child care centers (2%), and psychi-
atric care facilities (1%) comprised the remainder. Facility
type was not known for 4% of outbreaks tested. Mean age
of persons tested as part of an outbreak investigation was
82 years (SD 13.96 years) and median age was 85 years;
95% were >57 years of age.
Testing on the 589 specimens received from 161 out-
breaks registered from October 1, 2008 through June 12,
2009 was performed by real-time reverse transcription–
PCR (RT-PCR) for the infl uenza A virus matrix gene and
the Luminex Respiratory Viral Panel (RVP) (Luminex Mo-
lecular Diagnostics, Toronto, Ontario, Canada) for other
An etiologic agent was identifi ed in 89% of the 161
outbreaks tested by molecular methods. One-hundred-
eleven (69%) were caused by 1 etiologic agent. Two and
3 different pathogens were identifi ed in 24 (15%) and 6
(4%) outbreaks, respectively. Four pathogens were identi-
fi ed in 2 (1%) outbreaks. No etiologic agent was identifi ed
in 18 (11%) of the outbreaks tested by molecular methods,
which includes 1 specimen in which the result was indeter-
minate for coronavirus OC43. A wide range of causative
etiologic agents were detected for outbreaks by the RVP
assay (Table 2). Specimens from most patients were posi-
tive for enterovirus/rhinovirus (114 patients) followed by
metapneumovirus (85), parainfl uenza virus type 3 (55), and
human infl uenza virus A (H3) (41). No virus was identifi ed
in 186 patients.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 12, December 2009 2001
Author affi liations: Public Health Agency of Canada, Toronto,
Ontario, Canada (A. Marchand-Austin); and Ontario Agency for
Health Protection and Promotion, Toronto (D.J. Farrell, F.B.
Jamieson, N. Lombardi, E. Lombos, S. Narang, H. Akwar, D.E. Low,
Table 1. Respiratory outbreak submissions to Ontario, Canada,
public health laboratories by geographic location and season*
*Influenza season is delineated as October 1–April 19; spring season is
delineated as April 20–June 12.
†Specimens from 83 of the 112 outbreaks were tested by the RVP assay.
‡Greater Toronto Area includes submissions by Peel, York, and Toronto
Public Health Units.
§Specimens from 78 of the 101 outbreaks were tested by the Luminex
xTAG Respiratory Viral Panel (Luminex Molecular Diagnostics, Toronto,
Co-infections were noted in 22 of the patients tested by
the RVP assay. In 1 LTCF outbreak, 2 patients had co-in-
fection of an untypeable infl uenza A and enterovirus/rhino-
virus on testing by RVP. An infl uenza A real-time RT-PCR
result was negative in both patients; 1 patient had a co-in-
fection with respiratory syncytial virus B and enterovirus/
rhinovirus. Co-infections with coronavirus subtypes 229E
and NL63 were the most common, observed in 10 of the 22
patients (45%) infected with multiple pathogens. Isolates
from 1 patient were positive for 3 viruses (coronavirus sub-
types 229E and NL63 and enterovirus/rhinovirus).
One of the 2 outbreaks identifi ed as caused by pandem-
ic (H1N1) 2009 originated from a LTCF was not observed
until June 3, 2009, six weeks into the evolving pandemic,
despite widespread community prevalence. The second
pandemic (H1N1) 2009 outbreak, registered on June 11,
2009, originated from a hospital treating patients with infl u-
enza-like illness. Seasonal infl uenza (H1N1 and H3N2) or
pandemic (H1N1 2009) was detected in 2,966 (25.5%), and
pandemic (H1N1) 2009 in 2,203 (19%) of 11,612 persons
tested at PHL for infl uenza A by real-time RT-PCR dur-
ing April 20–June 12, 2009. Seasonal infl uenza A (H3N2)
was only identifi ed in 273 specimens (11.0%) of the 2,476
infl uenza A positive samples subtyped. However, it was the
strain responsible for 15 (88%) of the typeable infl uenza A
outbreaks at the same time. Seasonal infl uenza A (H1N1)
was absent from institutional outbreaks and only detected
in 41 (2%) of subtyped infl uenza A–positive samples from
the general population.
Persons with laboratory-confi rmed pandemic (H1N1)
2009 infection tested at the PHL, Ontario Agency for
Health Protection and Promotion, were younger than those
tested as part of outbreak investigations. Mean and median
ages were 21.5 and 16 years, respectively; only 10% were
>46 years of age.
The number of respiratory infection outbreaks in insti-
tutions submitted to PHL may refl ect disease impact caused
by respiratory viruses during the infl uenza season. Respi-
ratory viruses during the 2007–08 season may have been
more active than those of the 2008–09 season because the
number of outbreaks registered with PHL decreased from
1 year to the next. Declaration of pandemic status for the
novel (H1N1) virus has not infl uenced the reporting of re-
spiratory infection outbreaks from institutions in Ontario
because submission rates for the corresponding period in
2007–08 and 2008–09 are similar. Variation would not be
expected because reporting is required by Ontario law (4).
Respiratory viruses detected in outbreaks in institu-
tions refl ect those known to be major causes of acute respi-
ratory disease in the community; prevalence varies based
on geographic location, season, and detection methods
(5–7). Free access to such institutions by members of the
community (staff or visitors), in conjunction with commu-
nal close quarters of residents, creates an ideal environment
for propagation of viral respiratory outbreaks (8).
Current guidelines for isolation during viral respiratory
outbreaks are not tailored for the specifi c virus. As shown
in this study, multiplex molecular testing makes it possible
to identify the virus causing most LTCF respiratory infec-
tion outbreaks. Infection control guidelines for a specifi c
outbreak could be modifi ed based on the incubation period
and duration of viral shedding for the identifi ed virus (9).
The most commonly identifi ed virus in our study was
enterovirus/rhinovirus. Clinicians should be reminded that
2002 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 12, December 2009
Table 2. Etiologic agents identified by the Luminex Respiratory Virus Panel* from samples submitted by regional health units during
2009 spring outbreaks,
Ontario, no. (%)
Coronavirus OC43 1 (1)
Coronavirus NL63 0
Coronavirus 229E 4 (5)
Metapneumovirus 17 (20)
Respiratory syncytial virus A0
Respiratory syncytial virus B1 (1)
Influenza A (H3, human) 11 (13)
Parainfluenza 1 1 (1)
Parainfluenza 3 22 (27)
Enterovirus/rhinovirus 31 (37)
Pandemic (H1N1) 2009 virus 1 (1)
Invalid test¶ 0
Outbreaks tested 83
*Luminex Molecular Diagnostics, Toronto, Ontario, Canada.
†GTA, Greater Toronto area. Spring season is delineated as April 20–June 12; influenza season is delineated as October 1–April 19.
‡Iincludes submissions by Peel, York, and Toronto Public Health Units only.
§Seven of the 15 outbreaks were confirmed as rhinovirus by the Seeplex RV12 detection kit (Seegene, Inc., Seoul, South Korea).
¶Reported when the internal control is not detected during a run.
2009 spring outbreaks
GTA,‡ no. (%)
2008–2009 influenza season
outbreaks, GTA,‡ no. (%)
Respiratory Infection and Pandemic (H1N1) 2009 Download full-text
rhinovirus can cause severe lower respiratory tract infec-
tion, including death, as documented in several LTCF out-
breaks (10,11). These data highlight the need for molecular
capacity to diagnose rhinovirus infection because detection
is otherwise limited to less sensitive viral culture systems.
This review of outbreaks predominantly involving
elderly persons in LTCFs highlights the sparing of older
persons by pandemic (H1N1) 2009. Possible explanations
include cross-protective antibodies from previous expo-
sure to infl uenza A (H1N1) strains circulating before the
antigenic shift of infl uenza A to subtype H2N2 in 1957 or
minimal contact with those most likely to have imported
the pandemic strain into Canada (young travelers) (12). In
addition, older persons may have less contact with the age
group (children 10–19 years of age), with most cases being
in Ontario. Our fi ndings support Centers for Disease Control
and Prevention guidelines for vaccination with monovalent
pandemic (H1N1) 2009 virus vaccine. These guidelines
have not placed older persons in a high priority group for
vaccination because increased rates of hospitalization and
severe disease caused by pandemic (H1N1) 2009 have not
been observed (13,14). Investment in multiplex technolo-
gies to investigate respiratory outbreaks in LTCFs shortens
time for pathogen detection, helps guide infection control
and vaccination policies, and can potentially save resources
spent on other investigations.
We thank the Public Health Division, Ontario Ministry of
Health and Long Term Care, for assistance in identifying respira-
tory outbreaks during the study period.
Mr Marchand-Austin is a Liaison Technical Offi cer for the
province of Ontario, employed by the Public Health Agency
of Canada. This recently created position serves to facilitate
communication between provincial and federal public health
1. Monto AS. Epidemiology of viral respiratory infections. Am J
Med. 2002;112(Suppl 6A):4S–12S. DOI: 10.1016/S0002-9343
2. Gardner ID. The effect of aging on susceptibility to infection. Rev
Infect Dis. 1980;2:801–10.
3. Falsey AR, Treanor JJ, Betts RF, Walsh EE. Viral respiratory infec-
tions in the institutionalized elderly: clinical and epidemiologic fi nd-
ings. J Am Geriatr Soc. 1992;40:115–9.
4. Ontario Ministry of Health and Long-Term Care. Health Protection
and Promotion Act Ontario, Regulation 559/91. Specifi cation of Re-
portable Diseases [cited 2007 May 5]. Available from http://www.
5. Mahony JB. Detection of respiratory viruses by molecular methods.
Clin Microbiol Rev. 2008;21:716–47. DOI: 10.1128/CMR.00037-
6. Laguna-Torres VA, Gómez J, Ocaña V, Aguilar P, Saldarriaga T,
Chavez E, et al. Infl uenza-like illness sentinel surveillance in Peru.
PLoS One. 2009;4:e6118. DOI: 10.1371/journal.pone.0006118
7. Follin, P, Lindqvist A, Nyström, K, and Lyndh, M. A variety of re-
spiratory viruses found in symptomatic travellers returning from
countries with ongoing spread of the new infl uenza A (H1N1) virus
strain. Euro Surveill. 2009;14(24):pii 19242.
8. Nuno M, Reichert TA, Chowell G, Gumel AB. Protecting residential
care facilities from pandemic infl uenza. Proc Natl Acad Sci U S A.
2008;105:10625–30. DOI: 10.1073/pnas.0712014105
9. Lessler J, Reich NG, Brookmeyer R, Perl TM, Nelson KE, Cum-
mings DA. Incubation periods of acute respiratory viral infections:
a systematic review. Lancet Infect Dis. 2009;9:291–300. DOI:
10. Hicks LA, Shepard CW, Britz PH, Erdman DD, Fischer M, Flannery
BL, et al. Two outbreaks of severe respiratory disease in nursing
homes associated with rhinovirus. J Am Geriatr Soc. 2006;54:284–9.
11. Louie JK, Yagi S, Nelson FA, Kiang D, Glaser CA, Rosenberg J,
et al. Rhinovirus outbreak in a long term care facility for elderly
persons associated with unusually high mortality. Clin Infect Dis.
2005;41:262–5. DOI: 10.1086/430915
12. Centers for Disease Control and Prevention. Serum cross-reactive
antibody response to a novel infl uenza A (H1N1) virus after vacci-
nation with seasonal infl uenza vaccine. MMWR Morb Mortal Wkly
13. National Center for Immunization and Respiratory Diseases, Cen-
ters for Disease Control and Prevention (CDC). Use of infl uenza A
(H1N1) 2009 monovalent vaccine: recommendations of the Advi-
sory Committee on Immunization Practices (ACIP), 2009. MMWR
Recomm Rep. 2009;58(RR10):1–8.
14. Novel Swine-Origin Infl uenza A (H1N1) Virus Investigation Team,
Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, Garten RJ,
et al. Emergence of a novel swine-origin infl uenza A (H1N1) vi-
rus in humans. N Engl J Med. 2009;360:2605–15. DOI: 10.1056/
Address for correspondence: Jonathan B. Gubbay, Ontario Agency for
Health Protection and Promotion, Public Health Laboratory, Toronto,
Ontario M5G 1V2, Canada; email: firstname.lastname@example.org
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