epidemiology of community-acquired pneumonia in edmonton...

5
Can Respir J Vol 12 No 3 April 2005 139 Epidemiology of community-acquired pneumonia in Edmonton, Alberta: An emergency department-based study Thomas J Marrie MD, Jane Q Huang MApplSc Department of Medicine, University of Alberta, Edmonton, Alberta Correspondence and reprints: Dr Thomas J Marrie, 2J2.01 Walter C Mackenzie Health Sciences Center, 8440 112 Street, Edmonton, Alberta T6G 2R7. Telephone 780-492-9728, fax 780-492-7303, e-mail [email protected] TJ Marrie, JQ Huang. Epidemiology of community-acquired pneumonia in Edmonton, Alberta: An emergency department- based study. Can Respir J 2005;12(3):139-142. Patients aged 17 years and older who presented to seven emergency departments in Edmonton, Alberta over a two-year period with community-acquired pneumonia (n=8144) were studied. The admis- sion rates were 271/100,00 and 296/100,000 persons for year 1 and year 2 of the study, respectively. The admission rate increased with increasing age, peaking at 4639/100,000/year for those 90 years of age and older. In contrast, the percentage of patients who were admitted to an inten- sive care unit was highest for those in the younger age groups between 17 and 59 years of age. From 59 years of age and older, there was a pro- gressive decline in the percentage of patients admitted to an intensive care unit, with approximately 1% of those in the 90 years and older age group admitted. A pronounced seasonal effect on the number of patients presenting to emergency department was also noted. During the winter months, there was up to a 50% increase in the number of cases compared with the summer months. Key Words: Admission rate; Community-acquired pneumonia; Epidemiology Épidémiologie de la pneumonie extra-hospitalière à Edmonton en Alberta : Étude basée dans un service d’urgence Nous avons étudié les patients âgés de 17 ans et plus qui se sont présentés pour pneumonie extra-hospitalière dans sept services d’urgences d’Edmonton, en Alberta, au cours d’une période de deux ans (n=8 144). Les taux d’hospitalisation ont été de 271/100 000 et de 296/100 000 personnes pour l’an 1 et l’an 2 de l’étude, respectivement. Le taux d’hospitalisation augmentait avec l’âge avec une pointe à 4 639/100 000 ans pour les patients de 90 ans et plus. Par contre, le pourcentage de patients hospitalisés aux soins intensifs a été plus élevé chez les sujets plus jeunes, soit de 17 à 59 ans. À partir de l’âge de 59 ans, on a noté un déclin progressif du pourcentage de patients hospitalisés aux soins intensifs, 1 % environ des sujets de 90 ans et plus y ayant été admis. On a en outre noté un effet prononcé des saisons sur le nombre de patients qui ont consulté aux urgences. Au cours des mois d’hiver, une augmentation pouvant atteindre 50 % du nombre de cas a été enregistrée comparativement aux mois d’été. T here have been several population-based studies of the inci- dence of community-acquired pneumonia (CAP) (1-4). All of these studies have defined pneumonia on the basis of clinical features and the presence of an opacity on chest radi- ograph diagnosed as pneumonia by a radiologist (1-4). Population-based CAP studies are difficult to perform, and most studies have examined small populations. With chang- ing health care demands, there has been increased emphasis on treating as many patients as possible on an ambulatory basis. This form of care is ideally delivered in a family physi- cian’s office. However, up to one-third of the population in the Edmonton, Alberta area does not have a family doctor and these individuals often use the emergency department for routine medical care (5). Physicians in the emergency depart- ment often read the chest radiographs and make a diagnosis of pneumonia before receiving a radiologist’s interpretation. The objective of the current study was to define the epidemiology of CAP in an emergency department setting as diagnosed by emergency department physicians. A second objective was to determine the seasonal effect on the number of patients pre- senting to emergency facilities with pneumonia. METHODS Study sites Edmonton, Alberta, is a city of 666,505 adults aged 17 years and older that is served by six hospitals and one freestanding emergency room. There are two tertiary care hospitals, two hospitals that pro- vide secondary and some tertiary care, and two community hospitals. Study population and definition of CAP A pneumonia pathway consisting of components for managing pneumonia on an ambulatory basis and for managing pneumonia in patients requiring hospital admission was implemented November 15, 2000, and continued throughout the study at all hospitals and the one freestanding emergency department in Edmonton. Patients were enrolled into the pathway if they pre- sented to the emergency department at one of the seven sites with two or more symptoms or signs of CAP, plus radiographic evidence of pneumonia as interpreted by the emergency room physician or internal medicine consultant. Symptoms and signs of CAP included cough (productive or nonproductive), pleuritic chest pain, short- ness of breath, temperature higher than 38°C and crackles on aus- cultation. Patients were excluded from the pathway if they were thought to have aspiration pneumonia (year 1 only), tuberculosis, cystic fibrosis or if they required direct admission to the intensive care unit (ICU). Pregnant and nursing mothers and immunosup- pressed patients (greater than 10 mg/day of prednisone or other immunosuppressive drugs) were also excluded. Demographic, chest radiographic data and the reason for exclusion were collected on all patients who were not eligible for enrollment into the pathway. Patients from nursing homes were included as CAP. Patients who had been hospitalized within the previous two weeks were ©2005 Pulsus Group Inc. All rights reserved ORIGINAL ARTICLE

Upload: volien

Post on 19-Jun-2019

222 views

Category:

Documents


0 download

TRANSCRIPT

Can Respir J Vol 12 No 3 April 2005 139

Epidemiology of community-acquired pneumonia in Edmonton, Alberta:

An emergency department-based study

Thomas J Marrie MD, Jane Q Huang MApplSc

Department of Medicine, University of Alberta, Edmonton, AlbertaCorrespondence and reprints: Dr Thomas J Marrie, 2J2.01 Walter C Mackenzie Health Sciences Center, 8440 112 Street, Edmonton, Alberta

T6G 2R7. Telephone 780-492-9728, fax 780-492-7303, e-mail [email protected]

TJ Marrie, JQ Huang. Epidemiology of community-acquiredpneumonia in Edmonton, Alberta: An emergency department-based study. Can Respir J 2005;12(3):139-142.

Patients aged 17 years and older who presented to seven emergencydepartments in Edmonton, Alberta over a two-year period with community-acquired pneumonia (n=8144) were studied. The admis-sion rates were 271/100,00 and 296/100,000 persons for year 1 and year 2of the study, respectively. The admission rate increased with increasingage, peaking at 4639/100,000/year for those 90 years of age and older.In contrast, the percentage of patients who were admitted to an inten-sive care unit was highest for those in the younger age groups between17 and 59 years of age. From 59 years of age and older, there was a pro-gressive decline in the percentage of patients admitted to an intensivecare unit, with approximately 1% of those in the 90 years and older agegroup admitted. A pronounced seasonal effect on the number ofpatients presenting to emergency department was also noted. Duringthe winter months, there was up to a 50% increase in the number ofcases compared with the summer months.

Key Words: Admission rate; Community-acquired pneumonia;

Epidemiology

Épidémiologie de la pneumonie extra-hospitalièreà Edmonton en Alberta : Étude basée dans un service d’urgence

Nous avons étudié les patients âgés de 17 ans et plus qui se sont présentéspour pneumonie extra-hospitalière dans sept services d’urgencesd’Edmonton, en Alberta, au cours d’une période de deux ans (n=8 144).Les taux d’hospitalisation ont été de 271/100 000 et de 296/100 000personnes pour l’an 1 et l’an 2 de l’étude, respectivement. Le tauxd’hospitalisation augmentait avec l’âge avec une pointe à 4 639/100 000 anspour les patients de 90 ans et plus. Par contre, le pourcentage de patientshospitalisés aux soins intensifs a été plus élevé chez les sujets plus jeunes, soitde 17 à 59 ans. À partir de l’âge de 59 ans, on a noté un déclin progressif dupourcentage de patients hospitalisés aux soins intensifs, 1 % environ dessujets de 90 ans et plus y ayant été admis. On a en outre noté un effetprononcé des saisons sur le nombre de patients qui ont consulté auxurgences. Au cours des mois d’hiver, une augmentation pouvant atteindre50 % du nombre de cas a été enregistrée comparativement aux mois d’été.

There have been several population-based studies of the inci-dence of community-acquired pneumonia (CAP) (1-4).

All of these studies have defined pneumonia on the basis ofclinical features and the presence of an opacity on chest radi-ograph diagnosed as pneumonia by a radiologist (1-4).Population-based CAP studies are difficult to perform, andmost studies have examined small populations. With chang-ing health care demands, there has been increased emphasison treating as many patients as possible on an ambulatorybasis. This form of care is ideally delivered in a family physi-cian’s office. However, up to one-third of the population inthe Edmonton, Alberta area does not have a family doctorand these individuals often use the emergency department forroutine medical care (5). Physicians in the emergency depart-ment often read the chest radiographs and make a diagnosis ofpneumonia before receiving a radiologist’s interpretation. Theobjective of the current study was to define the epidemiologyof CAP in an emergency department setting as diagnosed byemergency department physicians. A second objective was todetermine the seasonal effect on the number of patients pre-senting to emergency facilities with pneumonia.

METHODSStudy sitesEdmonton, Alberta, is a city of 666,505 adults aged 17 years andolder that is served by six hospitals and one freestanding emergency

room. There are two tertiary care hospitals, two hospitals that pro-vide secondary and some tertiary care, and two community hospitals.

Study population and definition of CAPA pneumonia pathway consisting of components for managingpneumonia on an ambulatory basis and for managing pneumoniain patients requiring hospital admission was implementedNovember 15, 2000, and continued throughout the study at allhospitals and the one freestanding emergency department inEdmonton. Patients were enrolled into the pathway if they pre-sented to the emergency department at one of the seven sites withtwo or more symptoms or signs of CAP, plus radiographic evidenceof pneumonia as interpreted by the emergency room physician orinternal medicine consultant. Symptoms and signs of CAP includedcough (productive or nonproductive), pleuritic chest pain, short-ness of breath, temperature higher than 38°C and crackles on aus-cultation. Patients were excluded from the pathway if they werethought to have aspiration pneumonia (year 1 only), tuberculosis,cystic fibrosis or if they required direct admission to the intensivecare unit (ICU). Pregnant and nursing mothers and immunosup-pressed patients (greater than 10 mg/day of prednisone or otherimmunosuppressive drugs) were also excluded. Demographic, chestradiographic data and the reason for exclusion were collected on allpatients who were not eligible for enrollment into the pathway.Patients from nursing homes were included as CAP. Patients whohad been hospitalized within the previous two weeks were

©2005 Pulsus Group Inc. All rights reserved

ORIGINAL ARTICLE

Marrie.qxd 4/7/2005 2:37 PM Page 139

thought to have nosocomial pneumonia and no data were col-lected on these patients. Visits to the emergency room for pneu-monia within one month of the initial visit and re-admissionswithin two weeks of the initial admission were not included.

Six research nurses were hired to assist with the implementa-tion of the pathway and perform data collection.

Populations for which rates were calculated were defined asfollows:

• Definite pneumonia: all patients (both pathway andexcluded; ambulatory and admitted) who met the clinicalcriteria and had a chest radiograph read by a radiologist aspneumonia.

• Clinical pneumonia: all patients who met the clinicalcriteria and had a chest radiograph read by an emergencydepartment physician as pneumonia and by a radiologist asno pneumonia.

• Pneumonia requiring admission: all patients who wereadmitted including definite and clinical pneumonia.

• Pneumonia treated on an ambulatory basis: all patients whowere discharged from emergency to be treated at home.

• Pneumonia requiring admission to an ICU: patients withdefinite plus clinical pneumonia who were admitted to anICU.

Statistical analysisThe rate of admission for men was compared with that of womenusing the χ2 test.

The seasons were defined using the calendar definition,although cold weather (winter) starts in Edmonton in Novemberand ends in early April.

The Research Ethics Committee at the University of Albertain Edmonton, Alberta, approved the study.

RESULTSDuring the two years of the study, a total of 8144 patients hada diagnosis of pneumonia made in the seven emergencydepartments. Ninety-five per cent (7737 patients) were man-aged according to the pneumonia pathway. Five per cent(407 patients) did not qualify for the pathway.

Fifty-two percent (n=4259) of patients were treated on anambulatory basis and 42.7% (n=3478) were admitted to hospi-tal. Four hundred seven (5%) of the patients who were admit-ted to hospital were admitted to an ICU.

The overall admission rate per 100,000 adults for pneumo-nia was very similar for years 1 and 2 of the study at 271 and296, respectively. The rate for ambulatory pneumonia was sim-ilar for the two years at 289/100,000 and 315/100,000 persons,respectively. The age-specific admission rate was quite low upto 49 years of age; however, there were major increases in theadmission rate every five years thereafter, peaking at4639 admissions/100,000 persons in the 90 years and older agegroup. Figure 1 shows the age-specific admission rate in five-year intervals. Figure 1 also shows the rate of ambulatory pneu-monia by five-year age group. In Figure 2, the admission ratesare shown for women for both years of the study. Of note, therewas very little difference in the admission rates by study year.Figure 3 shows the admission rates for men and women foryear 1. From 70 years of age and older, the admission rates forpneumonia were significantly higher for men (P<0.01). Inyear 1, the rates were higher for pneumonia among women30 to 34 years of age, while there was no difference among theother age groups (Figure 3). In year 2, there was no difference

Marrie and Huang

Can Respir J Vol 12 No 3 April 2005140

0

500

1000

1500

2000

2500

3000

3500

4000

4500

5000

17-1

902-2

425

-92

30-3

453-3

904-4

454-4

950

-45

55-5

906-6

465

-96

70-

4775

-79

08-8

458-8

9 09+

Age group

per

,001 000

per

son

y raes

Admission year 1

Ambulaotry year 1

Admission year 2

Ambulaotry year 2

Figure 1) Admission rate and ambulatory pneumonia rate for patientswho presented to an emergency department with pneumonia duringyears 1 and 2

Figure 2) Total pneumonia (definite plus clinical) admission rate forwomen in years 1 and 2

0

500

1000

1500

2000

2500

3000

3500

4000

4500

71-1

902-2

425

-92

03-3

435

3-9

40-

4454-4

950

5-4

55-5

906-6

456-

9607-7

475

7-9

08-8

485

8-9

90+

Age group

per

1 0

,0p 000

erso

nraey s

Year 1

Year 2

0

1000

2000

3000

4000

5000

6000

7000

171-9

202-4

252-9

303-4

353-9

404-4

544-9

055-4

55-5

960

6-4

656-9

707-4

757-9

808-4

858-9 09

+

Age group

per

01 ,0

00p 0

erso

ny

raes

F

M

*

*

*

*

*

Figure 3) Total pneumonia admission rate for men and women in year 1.*Age groups for which the admission rate was higher for men thanwomen. F Females; M Males

Marrie.qxd 4/7/2005 2:37 PM Page 140

in the admission rate for men and women in the younger agegroups, while men were admitted at a higher rate at 50 to54 years of age and 60 years of age and older (data not shown).

Figure 4 shows the admission rates per 100,000 persons/yearwith pneumonia (all cases) and definite pneumonia to an ICU.The rate peaked for those patients who were 80 to 84 years ofage, at 202 cases/100,000 persons/year in year 1.

Figure 5 shows the percentage of patients with pneumoniaadmitted to an ICU by age group. The highest percentage ofpatients admitted to the ICU was in the younger age groups,from 17 to 59 years of age. For those 59 years of age and older,there was a progressive decline in the per cent of patientsadmitted to the ICU with pneumonia, with approximately1.4% of patients 90 years of age and older being admitted to anICU.

Figure 6 shows the percentage of patients who were admittedaccording to age group. Up to 49 years of age, 32% of all patientswho presented to the emergency departments and were diag-nosed with pneumonia were admitted. For those patients49 years of age and older, the percentage of patients who wereadmitted continued to increase, peaking at 76% to 77% forthose who were 90 years of age and older.

The seasonal effect on the number of patients with pneu-monia presenting to emergency departments is shown inFigure 7. Of note, the number of patients presenting to the

emergency department in the winter months was almost twiceas many as those who did so in the summer months

DISCUSSIONThis is the first comprehensive study examining the rate ofpneumonia presenting to emergency departments in a largeCanadian city. A unique feature of our study is the inclusion ofall patients with a clinical diagnosis of pneumonia. In a separatestudy that examined a subset of the current population ofpatients who were admitted to hospital, we found that patientswithout a radiographic diagnosis of pneumonia were older andhad a higher severity of illness score than those who had a radi-ographic diagnosis of pneumonia (6). The rates of bacteremia,positive sputum culture and mortality were similar in the twopopulations (6).

In a population-based study carried out in Finland (2), theincidence of pneumonia was 11.6/1000 persons/year. In theFinnish working population (ages 15 to 64 years), the meanannual hospitalization rate was 2.67/1000 persons for menand 1.10/1000 persons for women (3). The hospitalizationrate for all adult men and women in Edmonton was282/100,000 persons/year and 261/100,000 persons/year,respectively, in the first year of the study, and 329/100,000persons/year and 265/100,000 persons/year in the second yearof the study. Almirall et al (4) studied all persons 14 years of

Epidemiology of community-acquired pneumonia

Can Respir J Vol 12 No 3 April 2005 141

0

50

100

150

200

250

1-7

9102-2

42

-592

03-3

43

-593

04-4

44

-594

05-5

45

-559

06-6

46

-569

07-

4757-7

908-

4858-8

9 09+

Age group

per

,001 p 000

erso

nraey s

All pneumonia Year 1

Definite pneumonia Year 1

All pneumonia Year 2

Definite pneumonia Year 2

Figure 4) Intensive care unit admission rate for patients with pneu-monia (definite plus clinical pneumonia), and definite pneumonia inyears 1 and 2

0

5

10

15

20

25

30

35

40

17-1

920

-24

25-2

930

-34

35-3

940

-44

45-4

950

-54

55-5

960

-64

65-6

970

-74

75-7

980

-84

85-8

9

90+

Age group

Per

cen

atg

e%(

)

Year 1

Year 2

Figure 5) Percentage of patients with pneumonia who required admissionto hospital and were admitted to an intensive care unit in years 1 and 2

0

10

20

30

40

50

60

70

80

90

17-1

9

20-2

4

25-2

9

30-3

4

35-3

9

40-4

4

45-4

9

50-5

4

55-5

9

60-6

4

65-6

9

70-7

4

75-7

9

80-8

4

85-8

9

90+

Age group

%( egat

necreP

)

Year 1Year 2

Figure 6) Percentage of patients by age group who presented to anemergency department with pneumonia and were admitted to hospital

200

250

300

350

400

450

500

511/1

0/0

151/2

0/0

150/1

10/51

20//

10

51/

30/

10

510/4

0/1

150/5

0/1

150/6

10/51

70//

10

51/

80/

10

510/9

0/1

151/0

0/1

151/1

10/51

21//

10

5110//

20

5120//

20

150/3

0/2

150/4

20/

1550//

20

5160//

20

5170//

20

51/

800/2

150/9

20/

1501//

20

5111//

20

Time

Nu

mb

reo

fsesac

Figure 7) Number of persons with pneumonia by month fromNovember 15, 2000, to November 14, 2002

Marrie.qxd 4/7/2005 2:37 PM Page 141

age and older who were residents in the Maresme region inBarcelona, Spain. They excluded patients with nursing home-acquired pneumonia and aspiration pneumonia. The annualincidence of pneumonia in this study was 567 persons/100,000/year; however, 48% of all patients with pneumoniarequired admission to hospital. A generally accepted figure isthat 70% of patients with CAP are treated in the communityand 30% are admitted to hospital (5). In the current study,48% of the patients who presented to emergency departmentswere admitted to hospital. If we included all the patients whohad a diagnosis of pneumonia made in their physicians’ officesand walk-in clinics, the admission rate for pneumonia inEdmonton would likely be lower than the 30% quoted for theUnited Kingdom (5). In the United Kingdom, there are261,000 episodes of CAP each year, of which 83,153 (31.8%)are admitted to hospital (5).

It is noteworthy that another study carried out in Spainusing the national surveillance system for hospital data (7)indicated that the rate of hospitalization for pneumonia was1.6/1000 persons/year. Thus, it is likely that the rate of pneu-monia is low in Spain. A study that more closely resembles thecurrent study is that from Marston et al (8) who studied alladults residing in two counties in Ohio who were hospitalizedin 1991 for the treatment of CAP. The overall rate of hospi-talization was 260/100,000/year. The incidence was higheramong blacks at 337/100,000/year than among whites at253/100,000/year. Also, the incidence among men was higherthan among women, 291/100,000/year versus 244/100,000/year,respectively (8). Because the study by Marston et al includedonly patients who had chest radiograph-confirmed CAP (ourdefinite pneumonia), our rates of 220/100,000 and 180/100,000for definite pneumonia requiring admission to hospital foryear 1 and year 2 of the study are very similar.

Some striking findings from our study were the high rate ofadmission to an ICU for young persons who were admitted tohospital with pneumonia and the progressive decline in theadmission rate to intensive care for those 65 years of age andolder. In the Pneumonia Patient Outcomes Research Team(PORT) study (9) carried out in Boston, Pittsburgh and Halifax,

170 (12.7%) of the patients were admitted to an ICU for treat-ment of CAP (9); however, this was not a population-basedstudy. Moine et al (10) indicated that 18% to 36% of patientswho were admitted to hospital for the treatment of CAP requiredadmission to an ICU. Kaplan et al (11) conducted a study of allMedicare recipients hospitalized for the treatment of pneumoniain the United States in 1997 and found that the percentage ofpatients 65 years of age and older admitted to an ICU was 22.4%.The percentage of patients in our study who were 65 years of ageand older and who were admitted to ICU was 7.6%.

The seasonal effect on pneumonia admissions has beenknown for some time. In Finland, the peak months for theadmission of patients to hospital with pneumonia wereDecember and January and the months with the lowest admis-sions were July and August (12). Often, this seasonal increasecoincides with influenza activity in the community (13). It isnoteworthy that influenza activity was minimal in Edmontonduring the two years of the present study.

A strength of our study was the enrollment of all patientswho presented to an emergency department with pneumoniain a large city over two years. A weakness was that we did notstudy patients who were seen in physicians’ offices and werediagnosed with pneumonia; however, it is almost impossible todo this in such a large population. For this reason, enrolling allpatients who present to an emergency department in a citywith pneumonia is an attractive method for performing apopulation-based study. If such a method was embraced byother centres, we could readily compare the epidemiology ofpneumonia.

CONCLUSIONSThe pneumonia admission rates were remarkably stable over thetwo years of the study. As expected, the percentage of patientswho were admitted increased with increasing age. The effect ofage on admission to ICU was striking and unexpected, andrequires further study. The effect of climate on the number ofpatients with pneumonia presenting to an emergency depart-ment was considerable, with a major increase observed duringthe winter months.

Marrie and Huang

Can Respir J Vol 12 No 3 April 2005142

REFERENCES1. Foy HM, Cooney MK, Allan I, Kenny GE. Rates of pneumonia

during influenza epidemics in Seattle, 1964 to 1975. JAMA1979;241:253-8.

2. Jokinen C, Heiskanen L, Juvonen H, et al. Incidence of community-acquired pneumonia in the population of four municipalities ineastern Finland. Am J Epidemiol 1993;137:977-88.

3. Saynajakangas P, Keistinen T, Honkanen PO, Kivela SL.Hospitalization for pneumonia in the Finnish working-agepopulation. Cent Eur J Public Health 1997;5:27-9.

4. Almirall J, Bolibar I, Vidal J, et al. Epidemiology of community-acquired pneumonia in adults: A population based study. Eur Respir J2000;15:757-63.

5. Guest JF, Morris A. Community-acquired pneumonia: The annualcost to the National Health Service in the UK. Eur Respir J1997;10:1530-4.

6. Basi SK, Marrie TJ, Huang JQ, Majumdar SR. Patients admitted to hospital with suspected pneumonia and normal chest radiographs:Epidemiology, microbiology and outcomes. Am J Med 2004;117:305-11.

7. Monge V, San-Martin M, Gonzalez A. The burden of community-acquired pneumonia in Spain. Eur J Public Health2001;11:362-4.

8. Marston BJ, Plouffe JF, File TM Jr, et al. Incidence of community-acquired pneumonia requiring hospitalization. Results of active

population based surveillance study in Ohio. The Community-Based Pneumonia Incidence Study Group. Arch Intern Med1997;157:1709-18.

9. Angus D, Marrie TJ, Obrosky DS, et al. Severe community-acquired pneumonia: Use of intensive care services and evaluation of American and British Thoracic Society Diagnostic criteria. Am J Respir Crit Care Med 2002;166:717-23.

10. Moine P, Vercken JB, Chevret S, Gajdos P. Severe community-acquired pneumococcal pneumonia. The French Study Group ofCommunity-Acquired Pneumonia in ICU. Scand J Infect Dis1995;27:201-6.

11. Kaplan V, Angus DC, Griffin MF, Clermont G, Scott Watson R,Linde-Zwirble WT. Hospitalized community-acquired pneumonia in the elderly: Age- and sex-related patterns of care and outcomes in the United States. Am J Respir Crit Care Med 2002;165:766-72.

12. Sayanjakangas P, Keistinen T, Tuuponen T. Seasonal fluctuations inhospitalisation for pneumonia in Finland. Int J Circumpolar Health2001;60:34-40.

13. Upshur RE, Goel V. Measuring the impact of influenza on the hospital admission rates of the elderly in Ontario: A five-year admission rate analysis, 1988-1993. Can J Public Health2000;91:144-7.

Marrie.qxd 4/7/2005 2:37 PM Page 142

Submit your manuscripts athttp://www.hindawi.com

Stem CellsInternational

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Disease Markers

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation http://www.hindawi.com Volume 2014

Immunology ResearchHindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttp://www.hindawi.com Volume 2014

Parkinson’s Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttp://www.hindawi.com