Respiratory viruses in adults hospitalised with Community-Acquired Pneumonia during the non-winter months in Melbourne: Routine diagnostic ...
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2 0 19 Vo lum e 43 https://doi.org/10.33321/cdi.2019.43.12 Respiratory viruses in adults hospitalised with Community-Acquired Pneumonia during the non-winter months in Melbourne: Routine diagnostic practice may miss large numbers of influenza and respiratory syncytial virus infections. Lucy A Desmond, Melanie A Lloyd, Shelley A Ryan, Edward D Janus and Harin A Karunajeewa
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cdi.editor@health.gov.au.Original article Respiratory viruses in adults hospitalised with Community-Acquired Pneumonia during the non-winter months in Melbourne: Routine diagnostic practice may miss large numbers of influenza and respiratory syncytial virus infections. Lucy A Desmond, Melanie A Lloyd, Shelley A Ryan, Edward D Janus and Harin A Karunajeewa Abstract Background Community-Acquired Pneumonia (CAP) is one of the highest health burden conditions in Australia. Disease notifications and other data from routine diagnosis suffers from selection bias that may mis- represent the true contribution of various aetiological agents. However existing Australian prospective studies of CAP aetiology have either under-represented elderly patients, not utilised Polymerase Chain Reaction (PCR) diagnostics or been limited to winter months. We therefore sought to re-evaluate CAP aetiology by systematically applying multiplex PCR in a representative cohort of mostly elderly patients hospitalised in Melbourne during non-winter months and compare diagnostic results with those obtained under usual conditions of care. Methods Seventy two CAP inpatients were prospectively enrolled over 2 ten-week blocks during non-winter months in Melbourne in 2016-17. Nasopharyngeal and oropharyngeal swabs were obtained at admis- sion and analysed by multiplex-PCR for 7 respiratory viruses and 5 atypical bacteria. Results Median age was 74 (interquartile range 67-80) years, with 38 (52.8%) males and 34 (47.2%) females. PCR was positive in 24 (33.3%), including 12 Picornavirus (50.5% of those with a virus), 4 RSV (16.7%) and 4 influenza A (16.7%). CAP-Sym questionnaire responses were similar in those with and without viral infections. Most (80%) pathogens detected by the study, including all 8 cases of influenza and RSV, were not otherwise detected by treating clinicians during hospital admission. Conclusion One third of patients admitted with CAP during non-winter months had PCR-detectable respiratory viral infections, including many cases of influenza and RSV that were missed by existing routine clinical diagnostic processes. health.gov.au/cdi Commun Dis Intell (2018) 2019;43(https://doi.org/10.33321/cdi.2019.43.12) Epub 15/04/2019 1 of 11
Keywords: Lower Respiratory Tract Infection Methodology
(LRTI), Community-Acquired Pneumonia
(CAP) Polymerase Chain Reaction (PCR), Study Site and Population
Influenza, Respiratory Syncytial Virus
Patients admitted under the General Internal
Background Medicine (GIM) service at Sunshine and
Footscray campuses of Western Health, a 890
Community Acquired Pneumonia (CAP) is bed tertiary health service servicing >700,000
Australia’s sixth leading cause of death and the people in Western Melbourne. GIM manages
leading non-obstetric cause of hospital admis- approximately 70% of all CAP admissions
sion.1,2 A number of factors may have compro- (approximately 1000 per year).11
mised our understanding of CAP aetiology in
Australia. Firstly, information on the microbial Ascertainment and Eligibility
aetiology of CAP derived from notification data
and other routine diagnosis is compromised Participants were enrolled as a sub-study of
by selection and ascertainment biases, highly a currently ongoing health services improve-
variable approaches to diagnostic testing and ment program evaluation, “Evaluating the
the limited scope of existing surveillance and impact of a new model of care designed to
mandatory reporting processes. Secondly, most improve evidence-based management of com-
of Australia’s CAP healthcare burden manifests munity acquired pneumonia (IMPROVE-
in patients over age 65 who now account for 73% GAP)” (Clinical trials registration number:
of hospital bed stays for CAP.2 However this NCT02835040). IMPROVE-GAP prospectively
group has, in many ways been understudied identifies all GIM admissions (adults≥18) meet-
relative to younger, more diagnostically homo- ing a standardised case definition of CAP: new
geneous populations.3 Research studies of CAP evidence of consolidation on chest X-ray plus at
aetiology therefore risk under-representing the least one of cough, sputum production, dysp-
population in which the greatest burden occurs. noea, core body temperature ≥38.0C°, auscul-
Thirdly, previous Australian studies examin- tatory findings of abnormal breathing sounds
ing CAP aetiology have been limited mainly to or rales, leucocyte count >10,000/μl or-20°C. In subjects able to expectorate, sputum X-ray (based on the final radiologist report and
was stored at -20°C. Enrolment and sampling classified as “normal”, “new unilateral infiltrate”,
occurred on the first morning following admis- “new bilateral infiltrate” or “no new changes”).
sion (generally 12-24 hours after presentation)
and was performed independently of treating Statistical Analysis
clinical teams, regardless of whether or not
separate requests for PCR testing had already Study data were collected and managed using
been made through routine care processes. REDCap electronic data capture tools hosted
Research samples generated by this study were at The University of Melbourne. For analysis,
performed many weeks after collection so results all data was exported to Microsoft Excel and
were not available to clinicians in “real time” STATA (STATA Corp, version 14).
during the patient’s hospital stay. However,
for ethical reasons, positive results were com- Continuous variables are presented as mean ±
municated to treating clinicians and notified to standard deviation (SD) or, if non-normally
the Victorian Department of Health once they distributed, as median (range or interquartile
became available. range). Categorical variables are presented as
proportions (%).
Laboratory investigations
Results
Swabs and sputum specimens were evalu-
ated using a proprietary 16PLEX-PCR kit Patient characteristics
(Ausdiagnostics). The panel included res-
piratory viruses (Respiratory Syncytial Virus Of the 204 CAP patients admitted under GIM
(RSV), Influenza A, Influenza B, Parainfluenza, and enrolled in IMPROVE-GAP during the
Adenovirus, Human Metapneumovirus, recruitment periods, 114 (56%) were eligible
Picornavirus), Bordetella species (Bordetella of whom 72 (63%) consented to participate).
Pertussis, Bordetella Parapertussis) and Participants’ median age was 74 (interquartile
atypical bacteria (Mycoplasma pneumoniae, range 67 – 80 years). Those with a PCR-detected
Chlamydiaceae, Legionella species). We also influenza or RSV had similar baseline demo-
recorded when PCR testing was requested graphic and clinical characteristics to those
separately by the treating team as part of routine without (Table 1), although the influenza/RSV
care and whether infection prevention measures infection group was somewhat younger (62.8
were instituted. vs 73.9). Markers of disease severity at baseline,
including CORB score, CRP, white cell count
Additional demographic and clinical data and chest X-ray report were also broadly similar
in the two groups.
Prospectively collected data included demo-
graphic information, co-morbidities (including Pathogen prevalence by multiplex-PCR
19 co-morbidity groupings used to generate a
Charlson’s co-morbidity score12), vital signs, a A pathogen was detected in 24 individuals
pneumonia severity assessment (CORB score)11 (33.3%) including two with co-infections with
and a standardised symptomatology question- >1 virus. Because sputum samples were avail-
naire designed specifically for CAP (the CAP- able in only 11 (15%), most were detected in
Sym questionnaire)13. Results of all routine upper respiratory swab specimens. Oral and
investigations were also recorded including nasal swabs yielded concordant results for most
estimated glomerular filtration rate (eGFR), viruses (data not shown) except that of 4 RSV
C-reactive protein, white cell count and chest infections detected on oral swab, only one was
positive by nasal swab. Picornavirus was the
most commonly identified followed by RSV
health.gov.au/cdi Commun Dis Intell (2018) 2019;43(https://doi.org/10.33321/cdi.2019.43.12) Epub 15/04/2019 3 of 11Table 1: Baseline characteristics of 72 hospitalised adult patients with Community-Acquired Pneumonia according to presence or absence of
4 of 11
influenza or RSV.
Variable Influenza, rsv detected (N = 8) Influenza, rsv not detected (n = 64)
Age (years) 62.8 +/- 19.3 72.9 +/- 11.6
Sex male 6 (75.0) 32 (50.0)
Living in supported accommodation or aged care facility 1 (12.5) 6 (9.4)
Chronic obstructive pulmonary disease (copd) 4 (50.0) 41 (64.0)
Chronic cardiac failure (ccf) 1 (12.5) 19 (29.7)
Chronic kidney disease 0 (0) 6 (9.4)
Comorbidity Dementia 0 (0) 1 (1.6)
Diabetes 1 (12.5) 28 (43.8)
Myocardial infarction (mi) 2 (25.0) 17 (26.6)
≤2 6 (75.0) 34 (53.1)
Charlson cormorbidity index
>2 2 (25.0) 30 (46.9)
Number baseline medications 5.3 +/- 4.7 7.7 +/- 5.3
Egfr (ml/min/1.73M2) 73 [68.5 – 79.8] 67 [44.8 – 83.8]
C-reactive protein (mg/l) 87 [54.5 – 224.3] 114 [57.3 – 226.0]
Laboratory investigations White cell count (x109/l) 13.1 [9.9 – 16.9] 11.7 [9.9 – 15.9]
Mycoplasma (pcr and serology) 0 (0) 1 (1.6)
Clear lung fields 2 (25.0) 13 (20.3)
Commun Dis Intell (2018) 2019;43(https://doi.org/10.33321/cdi.2019.43.12) Epub 15/04/2019
New unilateral infiltrate 3 (37.5) 29 (45.3)
Radiologist’s chest radiograph
report New multilateral infiltrate 3 (37.5) 17 (26.6)
Nil new changes 0 (0) 5 (7.8)
≤1 6 (75.0) 48 (75.0)
Corb score
≥2 2 (25.0) 16 (25.0)
Data are mean +/- SD, median [interquartile range] or number (%).
health.gov.au/cdiFigure 1: PCR detection by pathogen in 72 participants hospitalised with CAP.
Respiratory Syncytial Virus
4 (6%)
Mycoplasma pneumoniae Influenza A*
1 (1%) 4 (6%)
Virus Detected Adenovirus*
No Virus Detected 23 (32%) 2 (3%)
48 (67%)
Picornavirus
12 (17%)
Parainfluenza*
2 (3%)
Human
metapneumovirus*
1 (1%)
* In two participants two viruses were detected (Parainfluenza & Influenza A, Adenovirus & Human Metapneumovirus) hence % does not
add up to 32%.
(four participants aged 32, 38, 69 and 87) and 0 of 46 (0%) blood cultures. No other pathogens
influenza A (four participants aged 59, 64, 72 were detected through investigations ordered by
and 81) (Figure 1). On further enquiry, 3 of clinical teams.
4 participants with positive influenza A PCR
had a recent history of international travel (all Symptomatology
recently returned from separate cruise ship
holidays). Mycoplasma pneumoniae was the CAP-Sym questionnaire responses in those with
only atypical bacteria detected by PCR (a single either influenza or RSV infections were broadly
case in a female aged 37 - confirmed by positive similar to those without (Figure 2).
Mycoplasma IgM). Serology (for Chlamydia,
Legionella pneumophila, Legionella longbeachae Comparison with viral testing
and Mycoplasma pneumoniae performed in 16) performed through routine clinical
and urinary legionella antigen testing (n=39) diagnostic practice
requested by treating teams (i.e. non-research
investigations performed at the discretion of Treating teams managing enrolled participants
clinicians) did not identify other possible atypi- requested viral PCR testing in only 4 patients,
cal bacterial infections. Bacteriologic investiga- yielding positive results in only one (parain-
tions performed by treating teams on the same fluenza) and instituted infection prevention
72 patients identified possible pneumococcal precautions (respiratory isolation) in only 3
infection in 1 of 23 (4%) sputum samples, 2 of 38 patients, including the sole parainfluenza PCR-
(5%) urinary pneumococcal antigen assays and positive patient and 2 others who had negative
PCR testing. Therefore, once results of research
testing had become available it became clear
health.gov.au/cdi Commun Dis Intell (2018) 2019;43(https://doi.org/10.33321/cdi.2019.43.12) Epub 15/04/2019 5 of 11Figure 2: CAP-Sym questionnaire responses in participants with influenza or RSV infections vs
those without influenza or RSV.
90
Influenza or RSV detected
80 Influenza or RSV not detected
Proportion of patients with a CAP-Sym score ≥ 3 (%)
70
60
50
40
30
20
10
0
Dyspnoea
Trouble Thinking
Cough
Chills
Nausea
Lack of Appetitie
Fatigue
Sputum
Haemoptysis
Sweating
Stomach Pain
Headache
Vomiting
Diarrhoea
Muscle Pain
Trouble Concentrating
Chest Pain
Trouble Sleeping
CAP-Sym Item Score (6-point scale)
that 23 PCR-positive participants, including ing this time of the year. Large recent increases
4 with influenza A and 4 with RSV had been in the numbers of Australians traveling to the
managed on the ward without respiratory pre- Northern hemisphere and tropical regions dur-
cautions, and had not been notified to public ing Southern hemisphere non-winter months
health authorities prior to these research results may also be a factor, as demonstrated by 3 of
becoming available. our participants with influenza having recently
returned from cruise ship holidays.
Discussion
Prevalence of respiratory viruses in CAP
This prospective study, performed in a repre- patients
sentative sample of hospitalised, mostly elderly
CAP patients in an urban Australian setting, By way of comparison, the most comprehen-
adds to existing information by demonstrating sive existing evaluation of CAP aetiology in
unexpectedly high overall rates of respiratory Australia is a multi-site study conducted over
virus detection in non-winter months. These 3 years (2004-2006) by the Australian CAP
included cases of RSV and influenza that Study (ACAPS) collaboration.4 Utilising a com-
appear to be being “missed” by routine clinical bination of PCR diagnostics and serology and
diagnostic processes and that therefore may be enrolling cases predominantly (>95%) in winter,
posing a previously under-recognized threat of they demonstrated an overall prevalence of res-
nosocomial infection. It suggests that the impor- piratory viruses of 15%, less than half that seen
tance of respiratory viruses in CAP during the in our study. Consequently, the much higher
non-winter months may be under-appreciated prevalence seen during non-winter months
simply because they are not being tested for dur- in our 2016/17 study was unexpected. Possible
6 of 11 Commun Dis Intell (2018) 2019;43(https://doi.org/10.33321/cdi.2019.43.12) Epub 15/04/2019 health.gov.au/cdiexplanations could include, firstly, that ours of symptomatology in predictive aetiological
was a relatively small study conducted over a diagnostic models for differentiating “viral”
6-month period at just 2 sites in close geographic from “non-viral” CAP27,28 and for “ruling-out”
proximity. Therefore, it may have reflected local influenza on purely clinical grounds.29-32 At our
or short-term epidemiological factors coinciding centre, as in most Australian hospitals, PCR
with our enrolment period. Secondly, our popu- testing for influenza and RSV is performed at
lation was generally somewhat older and with the discretion of treating clinicians. Therefore,
higher prevalence of co-morbidities than the individual clinicians are likely to base decisions
ACAPS study. This is consistent with previous on whether or not to test on their own perceived
data suggesting higher rates of virus detection “pre-test probability” of the likelihood of infec-
in elderly patients with CAP14,15 and may reflect tion. This perception may be influenced by (1)
a lower threshold for hospital admission in this the clinical symptoms and (2) epidemiological
group due to their underlying frailty. Thirdly, factors (such as the season during which the ill-
technical factors (related to specimen collection, ness occurs). Our study, together with existing
storage or the particular PCR platform used) evidence29-32, suggests the basis of this decision
may have influenced the diagnostic yields in the making may be flawed on both counts, as borne
two studies.16 out by the high proportion of “missed” cases of
influenza and RSV at our centre.
The observed difference in viral detection com-
pared with ACAPS was due mainly to the high Limitations and Strengths
rates of picornavirus in our study. Although
this might have reflected local factors, exist- Our study’s strengths included its use of a suit-
ing data suggests that although transmission ably representative population and systematic
peaks in winter, unlike influenza, year-round application of a consistent diagnostic strategy.
transmission is the norm.17-19 Moreover, studies In Australia, >70% of hospital bed occupancy
from Europe and North America have shown for adult CAP is in patients aged ≥70 and 55%
similar rates to ours, especially in elderly CAP in those ≥75.2 Therefore, our study’s median age
patients.20-23 The picornavirus genera (which of 74 whilst higher than in other studies4, was
includes rhinovirus) are generally considered representative of Australia’s true healthcare bur-
low-grade viral pathogens.18,24 Nonetheless it is den. By enrolling participants in the non-winter
notable that in the ACAPS study, of all patho- months, it addresses an important local knowl-
gens, the identification of picornavirus carried edge gap. However, caution should be exercised
the strongest association with requirement for in generalising its results due to its dual-centre
ventilator or vasopressor support.4 Other recent design, small sample size and narrow sampling
studies have described a higher mortality than timeframe. Also, because asymptomatic car-
with influenza in the hospitalised elderly.25 riage of many respiratory viruses is common,
assumptions regarding causality can be difficult
Symptomatology of viral infections. in a study such as ours that lacked a healthy
control group for comparison.
CAP can present with any combination of res-
piratory, gastrointestinal, neurological and sys- Conclusion
temic symptoms.26 We were able to characterize
these in a standardised way in our sample using This study adds to existing knowledge by detect-
an established, validated tool (the CAP-Sym ing viral respiratory pathogens in one third of
questionnaire). Although our sample size was adult patients admitted with a diagnosis of CAP
small, symptom patterns for the 18 individual under a GIM service during the non-winter
symptoms evaluated by CAP-Sym were broadly months. It reinforces how difficult, if not impos-
similar in those with and without influenza sible, it is to predict the presence of viral infec-
or RSV. This is consistent with the poor utility tions at the time of admission based purely on
health.gov.au/cdi Commun Dis Intell (2018) 2019;43(https://doi.org/10.33321/cdi.2019.43.12) Epub 15/04/2019 7 of 11symptomatology, existing routine diagnostic suggests it is important that review of current
tests and “seasonality”. It demonstrates how dis- hospital policy approaches should be considered
cretionary testing based on “clinical suspicion” for both winter and non-winter months.
can miss a large proportion of influenza and
RSV infections. These are highly transmissible List of abbreviations
in healthcare settings where they are associ-
ated with significant morbidity and mortality, Abbreviation Definition
especially in vulnerable populations such as the
ACAPS Australian CAP Study4
frail elderly admitted to GIM wards.6 Our study
adds to existing data suggesting that, rather CAP
Community Acquired
Pneumonia
than the application of clinical algorithms or
“discretionary” testing that have poor negative eGFR
Estimated Glomerular
Filtration Rate
predictive value, the only way to reliably exclude
these important potential agents of nosocomial GIM General Internal Medicine
infection in CAP patients is routine use of an “Evaluating the impact of a
appropriately high sensitivity diagnostic test.21,33 new model of care designed
However, at present complex issues of diagnostic to improve evidence-based
IMPROVE-GAP management of community
costs, diagnostic delay and other resource utili- acquired pneumonia”
sation implications (such as the availability and (Clinical trials registration
use of suitable isolation facilities) also need to be number: NCT02835040)
factored into the “risk-benefit equation” when PCR Polymerase Chain Reaction
considering alternative approaches. At our study RSV Respiratory Syncytial Virus
hospitals, like many others in Australia, the need
to institute respiratory isolation procedures in SD Standard Deviation
anyone tested for influenza (pending results that
may not be available for >24 hours) creates addi- Declarations
tional stresses on hospital resources, and can
therefore represent a perverse disincentive that Ethics approval and consent to
actually discourages testing. This may have been participate
a factor explaining the high numbers of “missed”
influenza and RSV in our study. Newer testing The study was approved by the Melbourne
platforms with more rapid turnaround times Health Human Research Ethics Committee
may help alleviate this problem but the clinical (MH2016.178).
utility and cost effectiveness of these tools has
not yet been reported. Our study suggests that Written informed consent was obtained from
a more comprehensive testing strategy (applying all participants. Patient anonymity is preserved
high sensitivity diagnostics to all CAP patients) within the text of this manuscript.
could unmask a currently hidden significant
disease burden and therefore could help reduce Consent for publication
risks of nosocomial infection. Our study also
Not applicable.
Competing interests
The authors declare that they have no competing
interests
8 of 11 Commun Dis Intell (2018) 2019;43(https://doi.org/10.33321/cdi.2019.43.12) Epub 15/04/2019 health.gov.au/cdiFunding 1. Department of Medicine, Melbourne Medi-
cal School – Western Health, University of
The study was supported by a grant from the Melbourne
HCF research foundation. The funder had
no role in study design or analysis. Harin 2. Western Health
Karunajeewa is supported by an Australian
National Health Medical Research Career 3. Department of Medicine, Melbourne Medi-
Development Fellowship. Melanie Lloyd is cal School – Western Health, University of
supported by an Australian Research Training Melbourne General Internal medicine Unit,
Scheme Scholarship. Western Health, St Albans, Vic
Authors’ contributions 4. Department of Medicine, Melbourne Medi-
cal School – Western Health, University of
LD coordinated data collection and participant Melbourne General Internal medicine Unit,
recruitment, analysed and interpreted data, Western Health, St Albans, Vic
and drafted and revised the manuscript. HK
conceived and designed the study, contributed 5. The Walter and Eliza Hall Institute of Medi-
to finalisation of the study protocol, analysis cal Research, Parkville
and interpretation of results, and revised the
manuscript for intellectually important con- Corresponding author
tent. EJ and ML contributed to the conception
and design of the study, coordinated the ethics Name: Lucy A Desmond
submission and statistical analysis, and assisted Postal Address: Western Health, 176 Furlong
with preparation of the manuscript. SR contrib- Road, St. Albans 3021
uted significantly to participant recruitment and Email Address: lucyannedesmond@gmail.com
data collection. All authors read and approved
the final manuscript. References
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