Abstract
The aim of the present study was to identify risk factors for community-acquired pneumonia (CAP), with special emphasis on modifiable risk factors and those applicable to the general population.
A population-based, case–control study was conducted, with a target population of 859,033 inhabitants aged >14 yrs. A total of 1,336 patients with confirmed CAP were matched to control subjects by age, sex and primary centre over 1 yr.
In the univariate analysis, outstanding risk factors were passive smoking in never-smokers aged >65 yrs, heavy alcohol intake, contact with pets, households with >10 people, contact with children, interventions on the upper airways and poor dental health. Risky treatments included amiodarone, N-acetylcysteine and oral steroids. Influenza and pneumococcal vaccine, and visiting the dentist were protective factors. Multivariable analysis confirmed cigarette smoking, usual contact with children, sudden changes of temperature at work, inhalation therapy (particularly containing steroids and using plastic pear-spacers), oxygen therapy, asthma and chronic bronchitis as independent risk factors.
Interventions for reducing community-acquired pneumonia should integrate health habits and lifestyle factors related to household, work and community, together with individual clinical conditions, comorbidities and oral or inhaled regular treatments. Prevention would include vaccination, dental hygiene and avoidance of upper respiratory colonisation.
Community-acquired pneumonia (CAP) remains an important cause of morbidity and mortality. Preventive strategies identifying and acting on modifiable risk factors are of paramount importance in reducing CAP-related death. Population-based studies of risk factors for CAP are scarce. In a Finnish study of subjects aged ≥60 yrs, alcoholism, heart disease, lung disease and immunosuppressive therapy, among others, were independent risk factors for pneumonia 1. Similar results were obtained in a study carried out in the UK, in which the importance of cigarette smoking was added 2. In a study carried out in Spain, other risk factors identified included low body mass index, previous respiratory infection and previous pneumonia 3. Some studies in USA population-based cohorts confirmed these findings and emphasised the influence of excessive weight gain, asthma and diabetes 4. Other risk factors for CAP suggested in these studies have been inconsistently observed or statistical confirmation was not possible. A systematic review of 10 studies analysing risk factors for CAP concluded that there is insufficient evidence for other factors, such as medication, dangerous substances, alcohol consumption or sociodemographic factors 5.
With the aim of providing further evidence on known and new risk factors for pneumonia, a large population-based study on CAP in adults was performed with special emphasis on the identification of modifiable risk factors and those applicable to the general population.
PATIENTS AND METHODS
Study population
A population-based, case–control study was conducted in an extensive area of the eastern coast of Spain, in which ∼95% of the population belongs to the National Health Care System, with public primary care centres and regional hospitals in each county. This is a mixed residential–industrial urban area with Mediterranean climatic conditions. The target population included 859,033 inhabitants aged >14 yrs assigned to any of the 64 primary care centres participating in the study. A total of 345 general practitioners were involved; the recruitment of the practitioners was made according to willingness to take part in the study. In order to demonstrate association with an odds ratio (OR) of 1.5 for risk factors for CAP with a prevalence of exposure in the control group of 5%, with 80% statistical power and significance level of 0.05, a sample of 1,500 cases and 1,500 controls was required.
Identification of cases
All patients with clinically suspected CAP presenting from November 1, 1999 to November 30, 2000 were prospectively registered. An active surveillance system was established to ensure the identification of all cases. This register involved all physicians working in public and private healthcare facilities in the study area and reference hospitals both inside and outside the county area of each primary care centre. In order to maintain the system of reporting cases, the coordinator in each of the study areas established periodic contact with responsible persons of all participating centres. Periodic meetings with all professionals involved in the study were also held.
Predefined criteria for case registration were based on acute lower respiratory tract infection for which antibiotics had been prescribed, in association with the appearance of previously unrecorded focal signs on physical examination of the chest and new radiological findings suggestive of pneumonia infiltrate 3. Criteria for clinical suspicion of acute lower respiratory tract infection included the presence of three or more of the following manifestations: cough with or without sputum production; dyspnoea and/or wheezing; pleuritic chest pain or abdominal pain; fever; headache; pneumonic consolidation on auscultation of the chest; sweating; arthromyalgias; dysphagia; and coryza. For clinically atypical CAP, one or more of the following criteria were considered: sweating; arthromyalgias; dysphagia; and coryza that required antibiotic prescription or persisted ≥5 days without antibiotics. In elderly patients, the possibility of pneumonia was also considered in the presence of prostration and/or anorexia and/or confusion or disorientation. In all cases in which criteria for clinical suspicion were met, a chest radiograph was ordered. Patients with initial doubtful radiographical images of CAP were tentatively included in the study and then excluded or definitively included according to clinical evolution and subsequent radiographical findings. All cases of CAP were re-evaluated by chest radiographs on the fifth day of illness and at monthly intervals until complete recovery.
Patients with aspiration pneumonia (witnessed aspiration with respiratory symptoms or oral content of aspiration) or active pulmonary tuberculosis, and patients who came from nursing homes or were discharged from hospital within 7 days of the onset of symptoms were excluded.
Selection of controls
Cases and controls were matched by sex, age (±5 yrs) and primary care centre. Frequency matching was performed. Cases were matched to controls in a 1:1 proportion. Controls were randomly selected from the list of subjects assigned to each primary care centre, and were recruited every 3 months. Controls who could not be contacted by telephone or home visits after three attempts were replaced following the same selection and matching criteria.
Data collection
A questionnaire on CAP risk factors was composed from the current literature and the opinion of international experts, the reliability of which has been demonstrated in previous studies 3, 6. It was administered directly to participants by trained physicians or nurses at home. The questionnaire included standardised information related to the following three aspects: 1) health habits and lifestyle, 2) clinical conditions and comorbidity, and 3) regular treatments during the last year. Items are briefly described in the Appendix. The complete questionnaire is available from the present authors upon request.
The study protocol was approved by the Ethics Committee of the Consorci Sanitari del Maresme (Barcelona, Spain) and all participants gave written informed consent before enrolment.
Statistical analysis
As a measure of association between risk factors and the occurrence of CAP, estimations of the relative risk through ORs and 95% confidence intervals (CI) were used. These were calculated using unconditional logistic regression. The Chi-squared test was used to assess differences between cases and controls in the frequency of variables related to health habits and lifestyle, clinical conditions and comorbidity, and regular treatments during the last year. All variables that were statistically significant in the univariate analysis with a p-value <0.10 were entered in a multivariable model with a stepwise approach. Moreover, it was considered appropriate to complement the multivariable analysis strategy by adjusting the effect of some drug treatments or vaccines for the underlying illness which were the reason for prescription. This focused on treatments for heart failure, respiratory diseases and the influenza and pneumococcal vaccines. In all cases, if multicollinearity among different variables was detected, the most generic variable was selected. No interaction assessment was systematically performed, due to the broad number of risk factors considered.
RESULTS
During the period of field work, 1,833 cases of clinical suspicion of CAP were identified, the diagnosis of which was not confirmed in 394 (21.5%). There were 1,439 patients with CAP, with an annual incidence rate of 1.54 cases per 1,000 inhabitants aged >14 yrs. A total of 2,107 control subjects were selected. The final study population included 1,336 patients with CAP and 1,326 controls. The distribution of cases and controls, and reasons for exclusion are shown in figure 1⇓. In the group of patients with CAP, 52.9% were males with a mean±sd age of 58.6±19.8 yrs and 47.1% were females aged 54.6±20.7 yrs. In the control group, 52.6% were males aged 58.9±19.6 yrs and 47.4% were females aged 54.6±20.6 yrs. Of the CAP patients, 61% were treated at home and the remainder were admitted to hospital.
Distribution of cases and controls. CAP: community-acquired pneumonia.
Univariate results
A comparison of health habits and lifestyle factors between cases and controls is shown in table 1⇓. Risk factors for CAP were as follows: underweight; different measures related to cigarette smoking; alcohol intake in males; contact with animals, excrements or visceras; sudden temperature changes in the workplace; living with >10 persons at home; usual contact with children; and contact with pets. Compared with never-smokers, both current smokers (OR 1.34) and ex-smokers (OR 1.37) showed a higher risk for CAP. Ex-smokers who had ceased smoking for >4 yrs showed a statistically significant reduced risk compared with ex-smokers of <1 yr (OR 0.39, 95% CI (0.17–0.89)). In the never-smokers aged >65 yrs, exposure to passive smoking was associated with a statistically significant increased risk for CAP (1.59 (1.02–2.48)). In males a statistically significant effect of the intensity of alcohol intake was observed above 40 g·day−1 (1.62 (1.10–2.39)). With regards to employment, building workers showed a higher risk for CAP (1.62 (1.15–2.28)) as did painters and carpenters (1.48 (1.10–2.0)). The greater the number of pets, the greater the risk for CAP (1.19 (1.097–1.30) for each additional animal).
Association between health habits and lifestyle factors and community-acquired pneumonia (CAP)
Risk factors for CAP related to clinical conditions and comorbidities are shown in table 2⇓. Previous hospital admission, previous CAP, history of upper respiratory tract infection, interventions on the upper respiratory tract (bronchoscopy, nasogastric tube), diabetes, heart disease, chronic bronchitis, asthma, nonactive pulmonary tuberculosis, epilepsy, chronic renal failure, cancer, HIV, dental dysaesthesia and dental prosthesis were risk factors for CAP. Visiting the dentist in the last month was a protective factor.
Association between clinical conditions and comorbidities and community-acquired pneumonia (CAP)
The bivariate effect of regular treatments is summarised in table 3⇓. Treatment with digoxin, amiodarone, diuretics, N-acetylcysteine, xanthines, oral steroids, inhaled steroids, inhaled β-agonists and inhaled anticholinergic drugs were risk factors for CAP. Moreover, the use of inhalers was a risk factor for CAP, particularly when medication was delivered through plastic pear-spacers or when medication contained steroids. Influenza and pneumococcal vaccines were protective factors.
Association between treatments and vaccinations and community-acquired pneumonia (CAP)
Multivariable results
Variables selected in the multivariable model (table 4⇓) included cigarette smoking, sudden temperature changes at work, contact with children, civil status, previous hospitalisation, history of upper respiratory tract infection, chronic bronchitis, asthma, epilepsy, oxygen therapy and use of inhalers with or without plastic pear-spacers. Visits to the dentist in the last month had a protective effect. In the multivariable strategy designed to adjust the effect of some drug treatments or vaccines for the underlying illness (table 4⇓), amiodarone and heart failure were statistically significant variables in the model of treatments for heart diseases, whereas N-acetylcysteine, inhalation therapy, oxygen therapy, chronic bronchitis and asthma were statistically significant factors in the model of treatments for respiratory diseases. Influenza vaccine was an independent protective variable for CAP but a statistically significant increased risk was observed in association with heart failure, chronic bronchitis, HIV infection and use of oral steroids. In relation to pneumococcal vaccine, pneumococcal vaccine was also an independent protective factor, although a statistically significant increased risk in association with heart failure, chronic bronchitis, asthma, HIV infection, oral steroids and radiation therapy or chemotherapy was found.
Risk factors for community-acquired pneumonia (CAP)
DISCUSSION
The present population-based study has provided an optimal framework to assess risk factors for CAP, in particular modifiable risk factors and those insufficiently proven in previous studies.
Being underweight was a risk factor for CAP, probably due to possible nutritional deficiency or associated diseases that may affect the immune system 7. In contrast to the study of Baik et al. 8, neither being overweight nor obese were associated with an increased risk of pneumonia. In the present study, as in others 6, 8, cigarette smoking was a risk factor for CAP. The present authors also found a statistically significant decrease in CAP risk in the second year following smoking cessation 8, which has been attributed to normalisation of immune and inflammatory function of lung tissue. Although other respiratory diseases in adults associated with exposure to environmental tobacco smoke have been reported 9, this is the first study showing a direct relationship between passive smoking and CAP in subjects aged >65 yrs.
High alcohol intake was an important risk factor for CAP 1; in males, alcohol consumption >40 g·day−1 had a statistically significant effect. Alcohol consumption was not a risk factor for CAP in females, maybe due to a lower prevalence of alcohol use or higher under-reporting. Heavy alcohol use causes alterations of the immune system, increasing host susceptibility to infectious diseases especially bacterial pneumonia 10. In other studies, however, a statistically significant effect of alcohol use has not been found, probably due to the lack of statistical power 3 or the inclusion of populations with low alcohol intake 8.
Exposure to certain environmental factors predisposes workers to occupational respiratory diseases 11. Contact with dust in the previous month, and some interrelated jobs (builders, carpenters, painters), were more frequent in cases than in controls, but in the multivariable analysis sudden changes of temperature in the workplace was the only independent environmental factor for CAP. It has been shown that inhalation of cold air causes cooling of the nasal epithelium, and that this reduction in nasal temperature is sufficient to inhibit respiratory defences against infection, such as mucociliary clearance and the phagocytic activity of leukocytes 12.
Living with >10 persons at home was associated with an increased risk for CAP. Contact with children was an independent risk factor in the multivariable analysis. Other studies have shown a higher incidence of CAP in adults with preschool children in the family, probably due to a higher carriage rate of Streptococcus pneumoniae 13. Contact with pets was also associated with an increased risk for CAP, which tended to be higher as the number of pets increased. This effect has only been previously observed in cases of psittacosis or zoonotic pulmonary infections 14. In relation to civil status, being single, widowed or divorced was independently associated with a higher risk for CAP than being married or living with a partner but the reasons for this finding are unknown.
Previous admission to hospital was associated with CAP independently of the patient’s comorbidity and other risk factors. This finding has been corroborated in other studies 15. Insertion of a nasogastric tube and the performance of a bronchoscopy can also be risk factors for CAP. A nasogastric tube favours bacterial growth and does not prevent oropharyngeal aspiration, and bronchoscopy may facilitate passage of oropharyngeal organisms to the bronchial tree 16. A very high risk of CAP associated with upper respiratory tract infections was observed 17, either presented in the previous month or repeated in the last year. Previous infection by respiratory viruses has long been regarded as a risk factor causing predisposition to pneumonia. A previous diagnosis of pneumonia, confirmed by radiographical findings, is also an independent risk factor for subsequent CAP. The risk increases with the number of previous CAP and recentness of infection. According to previous studies, an increased risk of CAP is maintained for at least 2 yrs following diagnosis 18.
With regard to underlying chronic diseases, patients with treated diabetes, heart disease, and nonactive pulmonary tuberculosis showed an increased risk. Heart failure and treatment with amiodarone were risk factors for CAP in the multivariable analysis. Treatment with amiodarone is associated with pulmonary toxicity, which may favour bacterial superinfection 19. Chronic bronchitis and asthma showed a strong relationship with CAP, which was independent of the remaining clinical factors and drug therapy.
In relation to regular treatments, N-acetylcysteine appeared as a statistically significant risk factor for CAP. In other studies, treatment with N-acetylcysteine was not effective for the prevention of acute exacerbations in patients with chronic obstructive pulmonary disease (COPD) 20. Oxygen therapy in the last year was selected as an independent risk factor in the multivariable analysis. Oxygen therapy may cause nasal and oropharyngeal dryness with difficulties in swallowing and favouring aspiration 21.
The use of oral and especially inhaled steroids was associated with CAP in the bivariate analysis. Other studies have shown an increased risk of pneumonia in patients treated with oral steroids 22 but evidence of the impact of inhaled steroids has not been previously documented, except as an unexpected finding in the Towards a Revolution in COPD Health (TORCH) study 23. The use of inhalers was also an independent risk factor for CAP. Poor hygienic measures and contamination of inhalers, particularly of plastic pear-spacers, is a recognised mechanism of infection 24. In addition, deep inhalation from pressurised aerosols may favour penetration of organisms from the oropharyngeal cavity to the bronchial tree. One of the most striking findings of the present study is that the risk of acquiring CAP was increased in patients using inhalers, especially with a chamber-spacer. When different medications were investigated, patients using inhaled steroids showed a higher risk compared with β-adrenergics and anticholinergics. These results fit well with the information provided by the TORCH study 23, in which patients treated with inhaled steroids (plus β-adrenergics) presented with a statistically significant higher risk of pneumonia when compared with those only treated with β-adrenergics. The present results highlight a predisposition to acquire pneumonia when using long-term inhaled steroids. Further research is definitely needed in this field.
A visit to a dentist in the last month was an independent protective factor for CAP. This finding may be related to better oral hygiene. Several studies provide evidence that the oral cavity may influence the initiation and/or progression of respiratory infections 25. In contrast, symptoms of dental dysaesthesia suggestive of dental caries and the use of dental prosthesis were associated with CAP in the bivariate analysis. In other studies, dental caries and periodontal disease were also associated with a higher probability of aspiration pneumonia by aspiration of contaminated saliva 12. Other factors facilitating aspiration and organisms reaching the lower respiratory tract are gastric acid-suppressive drugs. In a recent study, the use of proton pump inhibitors, especially when recently initiated, was associated with an increased risk of CAP 26. However, the present authors did not find a relationship between acid-suppressive therapy and CAP. Although bronchial aspiration was an exclusion criterion, it cannot be ruled out that some cases of silent undiagnosed aspiration as a cause of pneumonia could have been included. This may be the reason for the finding of epilepsy as a risk factor for CAP in the multivariable analysis. Conversely, dementia did not reach statistical significance, probably due to the lack of statistical power.
The effectiveness of the influenza vaccine in preventing CAP found in previous observational studies 27 was also confirmed by the present data. Regarding the pneumococcal vaccine, it should be noted that after adjusting for risk factors, which in turn were the reason for vaccination, the pneumococcal vaccine accounted for a 46% reduction in the risk of CAP. This finding is consistent with a previous study 28, although in another study the effect of pneumococcal vaccine in preventing CAP was not observed 29.
Finally, it has been suggested that inappropriate antibiotic treatment could be a risk factor for CAP, especially pneumonia caused by Legionella pneumophila or Chlamydia pneumoniae 30. In some patients who are smokers or who have chronic bronchitis, the use of antibiotics in the previous 3 months may determine a selection of respiratory flora, causing predisposition to opportunistic infection with colonisation of more aggressive organisms, which could be causative pathogens of CAP. The present study seems to support this hypothesis for cephalosporins and macrolides, a group of antimicrobials that is frequently used more indiscriminately.
The present results should be interpreted and take into account the influence of possible confounding factors and the presence of correlation between some of the analysed factors.
The current study provides useful clinical information to establish preventive interventions for community-acquired pneumonia in adults especially directed towards modifiable risk factors. Not only new risk factors, such as passive smoking, usual contact with young children, contact with pets or use of inhalers, have been identified, but also the statistically significant effect of other controversial factors in the literature, including pneumococcal vaccine, alcohol consumption and oxygen therapy, has been recognised. Timely medical care and preventive strategies directed towards the general population or those patients at risk are relevant measures for reducing the incidence of community-acquired pneumonia.
APPENDIX: ITEMS INCLUDED IN THE QUESTIONNAIRE
Identification and sociodemographic data
Identification number
Birth date
Sex
City
Date of the interview
Reason for not responding
Person who answered the questionnaire
Medical history
Hospital admission in the previous 5 yrs, number of admissions, date of the last admission
Diagnostic studies in the previous year: nose, pharynx, bronchoscopy, gastroscopy, nasogastric tube, general anaesthesia
Upper respiratory tract infection in the previous year, number of episodes, purulent tonsillitis
Upper respiratory tract infection in the previous month, number of episodes, purulent tonsillitis
Any previously radiographically confirmed pneumonia
Pathologic conditions
Diabetes, any diagnosis and treatment
Heart failure, any diagnosis
Valve heart disease, any diagnosis
Coronary heart disease, any diagnosis
Chronic bronchitis, any diagnosis; type of chronic obstructive pulmonary disease according to spirometry
Asthma, any diagnosis
Other chronic respiratory diseases (emphysema, bronchiectasis, etc.)
Nonactive pulmonary tuberculosis, any diagnosis
Epilepsy, any diagnosis
Parkinson’s disease, any diagnosis
Debilitating neuromuscular disorder (amyotrophic lateral sclerosis, multiple sclerosis, etc.), any diagnosis
Conditions involving the cranial nerves, any diagnosis
Dementia or Alzheimer’s disease, any diagnosis
Stroke, any diagnosis
Gastro-oesophageal reflux, any diagnosis; hiatal hernia, peptic ulcer
Chronic liver disease, any diagnosis
Hepatitis B or C virus infection, any diagnosis
Chronic renal failure, any diagnosis
Mental disorder or depression, any diagnosis
Tonsillectomy or adenoidectomy, any surgical removal
Cancer, type, any diagnosis, treatments in the previous year
HIV infection
Drug treatment
Regular treatments in the previous year: N-acetylcysteine, digoxin, amiodarone, diuretics, aminophylline, benzodiazepines, oxygen, inhalers with holding chamber (type and active drug), inhalers without holding chamber (type and active drug), antimicrobials (active compound)
Anthropometric and present conditions
Height and weight
Visit to the dentist in the previous month
Abscess
Edentulous
Caries
Dental prosthesis
Vaccinations
Influenzae in the previous year
Antipneumoccocal, year of administration
Toxic habits
History of tobacco use, to calculate pack-yrs
Passive smoking at work or home
Frequency of consumption of alcoholic beverages
Registration of consumption of alcoholic beverages, to calculate daily ingestion of pure alcohol (g)
Lifestyle and working conditions
Civil status
Living with >10 persons at home
Living or working with children aged <15 yrs
Pets, number and classes
Education level
Occupation (job)
Work-related contact with smoke, vapours, petrol or hydrocarbons, dust, organic fibres, inorganic fibres, ionised radiation, nonionised radiation, animals, excrements or visceras
Sudden changes of temperature in the work place in the previous 3 months
Support statement
This work received support from the Fondo de Investigaciones Sanitarias, Spanish Ministry of Health, grant FIS 99/0002-01, and CIBER Enfermedades Respiratorias 06/06/0028.
Statement of interest
None declared.
Acknowledgments
The authors would like to thank M. Pulido (freelance editor; Barcelona, Spain), for editing the manuscript and editorial assistance.
The members of the PACAP Study Group (Healthcare centres) are as follows. J.M. de Salas, J. Costa, M. Tristany, M.J. Grau, S. Sancho, E. Miguel, M. Fradera, I. Ochoa, M.J. Castany and A. Quilez (Health Basic Area of Arenys (Institut Català de la Salut (ICS)), Arenys, Spain); V. Marina, P. Subias, B. Jimeno, A. Bradnovich, M. Rodriguez, E. Ramon, A. Gardella and C. Ginés (Health Basic Area of Canet de Mar and Sant Pol de Mar (ICS), Canet de Mar, Spain); X. Mestres, A. Armada, J. Mallafré, M. Roger, M.T. Gros and N. Les (Health Basic Area of Ronda Cerdanya (ICS), Mataró, Spain); J. Joanola, J. Doménech, M. Bundó, M Trilla, J. Massons, J. Montero and E. Zurilla (Health Basic Area of Ronda Prim (ICS), Mataró, Spain); P. Torán, M.M. Aizpurua, G. Lozano, J. Casals, J. Sorribes and D. Torrellas (Health Basic Area of Gatassa (ICS), Mataró, Spain); J.L.L. Anglada, J. Salabarnada, E. Sanz, F. Gorgas, A. Ribas, E. Fau, I. Pellicer and S. Morales (Health Basic Area of Riera (ICS), Mataró, Spain); A. Casas, J. Bernad, A. de Montoliu, J. Gaya, R. Vallés, A. Vazquez, R. Peiró, G. Aresté, G.N. Mengual and M.C. Viñes (Health Basic Area of Vilassar de Mar (ICS), Vilassar de Mar, Spain); E. Almerich, M.A. Lopez, J. Bel, A. Gosalves, S. Macip, E. Carrillo, P. Paulo, M. Pol, J. Sala and P. Mir (Health Basic Area of Pineda (ICS), Pineda de Mar, Spain); P. Carrera, I. Legazpi, F. Planellas, A. Beltran, T. Planas, J. Rovira, M. De Ciurana, C. Xargay and R.B. Cortés (Health Basic Area of Sant Feliu de Guixols (ICS), Sant Feliu de Guixols, Spain); J. Paredes, J.G. Olive and P. Montoya (Health Basic Area of Hostalrich (ICS), Hostalrich, Spain); F.X. Burcet, D. Alcantarilla and J. de Ribot (Health Basic Area of Arbucies (ICS), Arbucies, Spain); M.R. Gorgot, R.A. Bas, M.B. Rosa and J. Castells (Health Basic Area of Sant Hilari Sacalm (ICS), Sant Hilari Sacalm, Spain); J.A. Castillo, J.C. Torrent, D. Rodríguez and X. Rius (Health Basic Area of Jaume 1 (ICS), Vilanova i la Geltrú, Spain); M. Navarro (Health Basic Area of Vilanova 1 (ICS), Vilanova i la Geltrú, Spain); J.M. Benet and J.C. Caballero (Health Basic Area of Roquetas (ICS), Sant Pere de Ribes, Spain); J. Llach, J. Sanglas and V. Morales (Health Basic Area of Vilafranca rural (ICS), Vilafranca del Penedes, Spain); J. Solanella (Health Basic Area of Piera (ICS), Piera, Spain); J.I. Cardona, J. Ferrer, M.J. Solís, F. Güerri, M.J. Murillo, M.D. Llovet, I. Guinea, M.M. Juáreztarrag, M. Alvarez, J. Bladé, I. Sánchez Oró, F. Martin, J.J. Cabré, J. Frigola, J. Boj, A. Chacon, E. Satué, F. Gallego, D. Montanyés, T. Basora, E. Martin, P. Gil, M. Roselló, J. Marimon, B. Costa, C. Gutiérrez, E. Moltó, A. Isach, N. Izzeddin, M. Campani, J. Ferré, A. Fernández, J. Jové, J. Vilalta, E. Ribera, M. Fernández, O. Ochoa, A. Vila Palacios and A. Donado-Mazarrón (Health Basic Area of Camp de Tarragona (ICS), Tarragona, Spain); C. Ramon, R. Caballol, L. Navarro, J. Masqué, L.L. Llor, G. Garcia, M.J. Arasa, A. Yoldi, I. Viloria, F. Vallespi, J.L.L. Clua, J.M. Basart, E. Ciurana, J.F. Monclus, A. Casanovas, L. Viñas, E. Checa, J. Marin, J. Santigosa and F. Arayo (Health Basic Area of Terres de l’Ebre (ICS), Tortosa, Spain); C. Campillos, A. Juarez and J. Perez (Health Basic Area of Tàrrega (ICS), Tàrrega, Spain); E. Paredes (Health Basic Area of Bages (ICS), Balaguer, Spain); J. Rodriguez (Health Basic Area of Cervera (ICS), Cervera, Spain); Y. Solà (Health Basic Area of Plà d'Urgell (ICS), Lleida, Spain); J. Pujol and M.A. Navarro (Health Basic Area of Lleida (ICS), Lleida, Spain); I. Casado (Health Basic Area of Balafia (ICS), Lleida, Spain); A. Vazquez (Health Basic Area of Eixample (ICS), Lleida, Spain); M. Madrid (Health Basic Area of Bordeta (ICS), Lleida, Spain); J. Berdié (Health Basic Area of Sallent (ICS), Sallent, Spain); M.J. Andrés (Health Basic Area of Suria (ICS), Suria, Spain); B. Barragan (Health Basic Area of Santa Eugenia de Berga (ICS), Berga, Spain); A. Torras (Health Basic Area of Tremp (ICS), Tremp, Spain); S. Gonzalez (Health Basic Area of Pont de Suert (ICS), Pont de Suert, Spain); A. Fuentes (Health Basic Area of Sant Joan de Vilatorrada (ICS), Sant Joan de Vilatorrada, Spain); J.A. El Hosn-Makarem, F. Pelaez and A. Ubieto (Health Basic Area of Breda, Breda, Spain); A. Fallada, A. Josa, E. Favà, M. Ros, M. Alonso, M.J. Pinazo, S. Borrás, J. Sala, C. Nolla, J. Bitrià and O. Araujo (Health Basic Area of Consorci Sanitari Santa Tecla, Tarragona, Spain); A. Collado and T. Glaria (Health Basic Area of SAGESA, Reus, Spain); J.C. Montero, P. Flores, P. Serra, E. Torrellas, I. Buxadé, J. Mussoll, M. Gomez, C. Serrano, M. Pubill and J. Gost (Health Basic Area of Cirera Molins (Consorci Sanitari del Maresme), Mataró, Spain); E. Burdoy, L.L. Busquets, S. de Castro, M. Bartolomé, E. Corona, R. Valverde and Y. Verde (Health Basic Area of Mataró Centre (Consorci Sanitari del Maresme), Mataró, Spain); M. Alegre, M. Papiol, O. Martí, M. Catalá, M.A. Martinez, A. Casanovas and E. Diaz (Health Basic Area of Argentona (Consorci Sanitari del Maresme), Argentona, Spain); A. Borrás and F. Aznar (Centre Mèdic de Mataró, Mataró, Spain); F. Riera, A. Vazquez and P. Gil (GEMA S. L., Mataró, Spain); J. Costa, I. Colom, E. Calvet, J. Nicolás, J. Ruiz (Health Basic Area of Lloret-Tossa (Corporació de Salut del Maresme i la Selva), Lloret de Mar, Spain); C. Mateu (Health Basic Area of Son Serra-La Vileta (Servei de Salut de les Illes Balears (IB-SALUT)), Mallorca, Spain); J. Arranz (Health Basic Area of Arquitecte Bennassar (IB-SALUT), Mallorca, Spain); A. Fé (Health Basic Area of Escola Graduada (IB-SALUT), Mallorca, Spain); B. Puig (Health Basic Area of Coll d'en Rabassa (IB-SALUT), Mallorca, Spain); M. Gutiérrez (Health Basic Area of Santa Catalina (IB-SALUT), Mallorca, Spain); L.L. Morant (Health Basic Area of Felanitx (IB-SALUT), Mallorca, Spain); M. Llull and J. Estelrich (Health Basic Area of Son Gotleu (IB-SALUT), Mallorca, Spain); L. Quintana (Health Basic Area of Marines-Muro (IB-SALUT), Mallorca, Spain); C. Llabrés (Health Basic Area of Emili Darder (IB-SALUT), Mallorca, Spain); M.M. Sureda (Health Basic Area of Son Cladera (IB-SALUT), Mallorca, Spain); L. Cuevas (Health Basic Area of Pere Garau (IB-SALUT), Mallorca, Spain); Y. Muñoz and J. Llobera (IB-SALUT, Mallorca, Spain); M. Iñiguez, J. Guasch, F. Sánchez, J. Pascual, A. Castelló and L.L. Gómez (Health Basic Area of IB-SALUT, Menorca, Spain); P. Marin, C. Garcia and P. Moreno (Health Basic Area of INSALUD, Valencia, Spain); M. Coll, C. Palma and C. Ribera (Àrea de Vigilància Epidemiològica del Ministeri de Salut, Benestar Social i Família del Govern d'Andorra, Principality of Andorra); J. Aldosa, C. Alonso, A. Bergés, J. Burgués, L.L. Burgués, J. Busquets, D. Casal, N. Cerdán, X. Crespo, R. Duat, J. Escoda, M. Fiter, A. Font, M. Fraysse, S. Fuentes, R. García-Núñez, T. López-Pinacho, M. Masardo, J. Martínez-Illescas, P. Morisset, M. Pallarés, R. Pérez-Serra, A. Plà, E. Pons, A. Ruiz, J.C. Rodríguez-Picart, J. Sánchez-Claver, E. Sylvestre, R. Tolosa, J.A. Touceda, J.R. Varela and J.C. Vidal (Health Basic Area of Associació Andorrana de Metges d'Assistència Primària, Principality of Andorra).
The participants from hospital centres were: O. Parra (Hospital Universitari del Sagrat Cor, Barcelona, Spain); F. Riera (Hospital de Barcelona, Barcelona, Spain); G. Pera, E. Palomera, J. Bigas, H. Pelaez, E. Coma, M. Daza, F. Casarramona, J. Bassa and X. Balanzó (Hospital de Mataró (Consorci Sanitari del Maresme), Mataró, Spain); P. Tudela (Hospital Universitari Germans Trias i Pujol, Badalona, Spain); R. Tarradas and M. Berrocal (Hospital Sant Jaume, Calella, Spain); J. Requena (Hospital Pius de Valls, Valls, Spain); M. Amate, C. Bara, O. Becerra, R. Bellmunt, F. Boneu, J. Bozal, C. Burillo, A. Díaz, N. González, A. Granyena, M. Gutiérrez, C. Infante, M. Leal, M. Linares, J. Magallón, J. Marqués; M.J. Martí, J.C. Miralles, C. Mora; J.M. Palacín, J. Pons, G. Prats, G. Pujal, M. Sanjuán, X. Segarra, J. Solís, H. Trelles, G. de Celis, X. Latorre, O. Sarroca and H. Briceño (Hospital Nostra Senyora de Meritxell (SAAS: Servei Andorrà d'Atenció Sanitària), Principality of Andorra).
Footnotes
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Earn CME accreditation by answering questions about this article. You will find these at the back of the printed copy of this issue or online at http://www.erj.ersjournals.com/current.shtml
- Received July 27, 2007.
- Accepted January 9, 2008.
- © ERS Journals Ltd
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