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Clinical Investigations: ASTHMA |

Variations in Pediatric Asthma Hospitalization Rates and Costs Between and Within Nordic Countries* FREE TO VIEW

Vasilisa Sazonov Kocevar, MPharm, PhD; Hans Bisgaard, MD, DMedSci; Linus Jönsson, MD, MSc; Erkka Valovirta, MD, PhD; Frederik Kristensen, MD, MPH; Donald D. Yin, PhD; Joseph Thomas, III, PhD
Author and Funding Information

*From the Department of Paediatrics (Dr. Bisgaard), Danish Paediatric Asthma Center, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark; Department of Pharmacy Practice (Drs. Kocevar and Thomas), Purdue University, West Lafayette, IN; Stockholm Health Economics (Dr. Jönsson), Stockholm, Sweden; Turku Allergy Center (Dr. Valovirta), Turku, Finland; PharmEcon AS (Dr. Kristensen), Asker, Norway; and Merck & Co. (Dr. Yin), Whitehouse Station, NJ.

Correspondence to: Hans Bisgaard, MD, DMedSci, Professor of Paediatrics, Danish Paediatric Asthma Centre, Department of Paediatrics, L213, Copenhagen University Hospital, Niels Andersens Vej 65, Gentofte, DK-2900 Copenhagen, Denmark; e-mail: bisgaard@copsac.dk



Chest. 2004;125(5):1680-1684. doi:10.1378/chest.125.5.1680
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Published online

Background: We assessed variations in hospitalization parameters and costs among asthmatic children in four Nordic countries by geographic location and age groups.

Methods: Cross-sectional, county-level aggregate data on asthma-related hospitalizations in 1999, obtained from public national databases for children < 15 years old from Denmark, Sweden, Norway, and Finland, together with country-specific asthma management cost were used to estimate the incidence of first hospital admission (per 1,000), length of hospital stay (LOS), and hospitalization cost. Longitudinal patient-specific data from 1998/1999 were used to calculate the relative hazard of readmission (RHR) using a multivariate Cox proportional hazards model.

Results: Nordic incidence of first hospital admission in 1999 was 2.17 per 1,000 children, readmission was noted in 16% of the patients, mean LOS was 2.64 days, and total hospitalization cost was almost $14 million. Hospitalization incidence, RHR, and costs were significantly higher in children < 5 years old compared with school children 6 to 14 years old. Hospital LOS, incidence of first hospital admission, and cost per child were the highest in Denmark, though RHR did not differ significantly from Sweden.

Conclusions: Large variations in all parameters were observed between and within countries. Given the similarities among the four countries studied, these results may, among other reasons, indicate different efficiencies of the various asthma management plans between and within them. The presented measures of hospitalization patterns could prove to be valuable quality-of-care measures to guide further improvements in asthma management.

One of the main goals of long-term asthma management is to avoid asthma-related hospital admissions, which remain the second most common cause of hospitalizations in children.13 In addition, hospitalization costs account for 46 to 74% of the total direct cost of asthma management in the United States and Europe.48 Significant reductions in hospitalization and readmission rates have been reported during the recent decade from Denmark,9and also from local regions within other Nordic countries.1011 However, a large proportion of children is still hospitalized each year despite extensive educational programs and use of preventive drugs, and the rate of variation within and between national health-care systems remains unknown.2 Denmark, Sweden, Norway, and Finland are relatively homogeneous in terms of culture, sociodemographic characteristics, and access to publicly funded care. Validated nationwide inpatient registries, based on the International Classification of Diseases (ICD), 10th Revision, and used for prospective hospital financing and policy development, also are available throughout the region, creating a favorable setting for clinical and health-services research.

The objective of this study was to assess variations in asthma-related hospitalization patterns between and within Nordic counties, as well as between age groups. Incidence of first hospital admissions, length of hospital stay (LOS), hospitalization costs, and relative hazard of readmission (RHR) were used to reflect the patterns of hospitalization. Such measures may be useful to evaluate and guide improvement in quality of care and asthma management plans, which have previously been shown, together with other factors, shown to significantly impact the rate of asthma-related hospital admissions.24,7,12

The study was designed as a 12-month retrospective database analysis on a regional, national, and overall Nordic level assessing inpatient resource use in Denmark, Sweden, Norway, and Finland in 1999. Two types of data on asthma-related hospitalizations were obtained from publicly available national inpatient registries (Danish National Board of Health and Welfare, Norwegian Patient Register, Finnish National Research and Development Centre for Health and Welfare, and Swedish National Board of Health and Welfare) for children < 15 years old. The first source included data on county-level aggregate inpatient services use according to gender and three age groups (< 2 years [infants], 2 to 5 years [young children], and 6 to 14 years [schoolchildren]) from Denmark, Sweden, Norway, and Finland. Variables requested from these validated databases, which routinely collect inpatient resource use (via ICD codes recorded by doctors) from all hospitals nationwide and link it to patient identifying numbers and sociodemographic characteristics, were the number of children hospitalized, the number of hospital admissions (hospital episodes), and bed days incurred. Populations included children whose primary reason for admission was asthma related as defined through ICD, 10th Revision codes. These included J45.0 (mainly allergic asthma), J45.1 (nonallergic asthma), J45.8 (mixed asthma), J45.9 (unspecified asthma), and J46.x (acute severe asthma). A second (longitudinal) source of data were patient-specific hospitalizations for asthma in 1998 and 1999 obtained from Sweden, Denmark (ICD 10th Revision), and Norway (ICD, Ninth Revision in 1998, ICD, 10th Revision in 1999), including the following variables: date of hospital admission, gender, age at first hospital admission, county of residence, and county of the hospital. Data in national inpatient registries are periodically checked for quality of diagnostic codes and identifying numbers for patients.

Data sources on cost per asthma episode were obtained from the Ministries of Health in respective countries, which routinely collect data for prospective budgeting purposes. The total number of children living in each county and country was obtained from the national statistical institutes for 1999, where centralized population census serves as a data collection tool. Counties were first classified into either urban or rural, according to the population density and presence of major urban centers, and later grouped into geographic regions.

The following calculations were based on aggregate inpatient data provided by national inpatient registries. The age group-specific incidence of first hospital admissions in 1999 was calculated for each region and country by dividing the total number of first hospitalizations in 1999 with the number of children living in the respective areas standardized per 1,000. The average LOS per hospitalization was estimated by dividing the total number of bed days with the total number of hospital episodes in each region and country. χ2 proportional tests were carried out in order to assess possible association between LOS > 2 days and gender, age groups, and location (urban/rural). The cutoff was selected according to the mean LOS in the Nordic region, rounded to the whole number due to the discrete nature of the variable.

The total annual hospitalization cost for each region and age group was calculated by multiplying the total number of bed days with a unit cost per bed day. To estimate the latter in each country, we obtained asthma-related hospitalization cost and average LOS for patients hospitalized under the diagnosis related group (DRG)-98 (asthma and bronchitis in patients < 18 years old) for 1999. The unit cost per bed day was then calculated by dividing total DRG-98 hospitalization cost by average LOS for the DRG. All currency conversions were based on the purchase power parity exchange rate in 1999. Any differences in resource utilization found among the care-seeking populations across countries were definitive and did not require further statistical inference in order to draw conclusions, as we were working with the entire pediatric population with asthma and not samples.

The longitudinal, patient-specific data from Sweden, Denmark, and Norway were used to assess the RHR, defined as a separate admission to the hospital > 1 week after the first asthma discharge during the study period. At least 7 days between the hospitalizations were required in order to ensure that the second hospitalization was a consequence of a new exacerbation and not administrative transfer/shifting between departments (eg, emergency department to pediatrics) during the same episode. Ex ante sensitivity analysis revealed no significant differences in rate of rehospitalization when required gap was varied between 1 day and 7 days. The Cox proportional hazards model was used to estimate the RHR between age groups, regions and countries, controlling for asthma type (based on ICD, 10th Revision) and gender. The response variable was the length of time between subsequent hospitalizations during a 2-year period. Cox modeling is a semiparametric method, which uses the data on patients whose event of interest has occurred (eg, second hospitalization in a given time period), and also on patients who did not experience the event of interest (censored patients). It accounts for the timing of the outcome variable, such as second hospitalization in our example, vs regular nonlinear multivariate models, which only account for whether the event of interest occurred or not.

Among 4,437,254 children < 15 years old in the four Nordic countries in 1999, 9,635 children (0.22%) were hospitalized due to asthma at least once during 1999, with a total of 11,484 hospital admissions and 30,264 bed days. Among previously hospitalized children, 15.7% were readmitted within the 2-year period. Mean LOS for Nordic children < 15 years of age was 2.64 days in 1999. The total annual costs of asthma-related hospitalizations were $4.9 million, $3.6 million, $3.7 million, and $1.9 million in Denmark, Finland, Sweden, and Norway, respectively. Overall cost per bed day was estimated as $456 in US dollars ($1 = 8.58 Danish krona) in Denmark, $498 in US dollars ($1 = 9.78 Swedish krona) in Sweden, $581 in US dollars ($1 = 6.15 Finnish marks) in Finland, and $304 in US dollars ($1 = 9.49 Norwegian krona) in Norway.

The incidence of first hospital admissions, LOS, hospitalization cost, and RHR are given by geographic location in Table 1. Large variations in these measures of hospitalization patterns were observed between and within the countries. χ2 tests showed no consistent pattern in LOS regarding rural vs urban areas nor gender. Denmark presented with the highest figures regardless of the measure, apart from the nonsignificantly higher RHR in Sweden. (Table 1).

The youngest children (< 2 years) were the highest users of health-care resources due to more common first admissions as well as readmissions (Table 2). However, schoolchildren in Denmark and Finland were 2 times and 1.4 times more likely (p < 0.0001) to have longer LOS, respectively, than children aged ≤ 5 years. Overall on the Nordic level, the youngest children (< 2 years) consumed approximately 8.5 times more per capita for inpatient health care due to asthma compared to school children, and 2 to 5 year olds consumed approximately 2.8 times more than school children.

This is the first study to compare asthma-related hospitalization patterns between and within Nordic countries. We found marked variations in the rate of asthma-related hospitalizations, LOS, and cost, both between and within countries. There was no consistent difference in terms of utilization between rural and urban areas, or gender. Denmark incurred the highest incidence of first hospital admissions as well as cost per capita, with large variations within the country, while Sweden incurred the highest RHR numerically, though not statistically different from RHR in Denmark. Variations were also observed with respect to age group. Children < 2 years old had the highest hospitalization rates, cost per capita, and RHR readmission. Children < 5 years of age consumed 75% of the total pediatric inpatient resources for asthma management in the Nordic region.

Hospitalization rates may reflect reliance on hospitalization for asthma management and/or a lower level of asthma control in the primary care setting. Lack of disease control at the primary care level often results in higher hospital utilization.24,7,12 We previously introduced readmission rate as a measure of the efficiency of asthma management in the secondary care setting.9 Once the child has been hospitalized, it is largely a failure of the secondary care if readmission for asthma is needed. Hospital LOS also may reflect the efficiency of hospital-based asthma management. In this study, LOS showed geographic variations in concordance with the differences in hospital admission rates and RHR, which supports the validity of these measures.

Hospitalization rates, RHR, and cost were higher among younger children, which is consistent with other studies1011,13 that reported higher resource utilization among younger patients. Our findings suggest that the hospitalization rate among children < 2 years old was 2.3 times higher than for 2- to 5-year-olds, which was four times higher than for children aged 6 to 14 years. This is partly a consequence of the disease prevalence and onset, but also may be a reflection of the disease management at the primary level. Asthma has an early onset, usually with symptoms of low specificity. In addition, the management of very young asthmatic children lacks the evidence base and consensus available for management of older children. These factors may have caused the observed greater resource use among younger children. To exclude the possibility that younger children were experiencing more severe asthma on average, we examined the proportion of children by age group and country, admitted according to specific ICD codes adjusted for severity (J46.x). This subanalysis revealed that a smaller proportion of younger children actually had severe asthma at hospital admission in all countries. Children who were admitted due to any other asthma-related diagnosis not described with ICD codes J45.x and J46.x were not included in our study, and therefore those diagnoses (eg, bronchiolitis, wheezing bronchitis) could not account for hospitalizations in our population.

Large regional variations in hospitalization patterns found in this study are surprising in view of the sociodemographic, health status, and health-care system similarities among the four Nordic countries. Indicators like gross domestic product, percentage of gross domestic product spent on health care, public spending for health care per inhabitant, proportion of urban population, infant mortality rate, life expectancy at birth, and the number of physicians per 100,000 inhabitants, are very similar for the Nordic countries.1415 In addition, asthma-specific mortality rates and access to specialist care as approximated by the presence of pediatric departments do not vary substantially.1618 The prevalence of asthma in children also has been shown to be similar between countries, as well as between regions within Norway19and Sweden.20Our data indicate that according to the ICD coding system, the proportion of children with severe asthma at hospital admission is similar among the four countries studied. Finally, the association between poverty and asthma severity is inconsistent.21 Even if evidence was pointing into any particular direction, due to similar distribution of sociodemographic and clinical characteristics of the asthmatic children in Nordic countries, we have no reason to believe that these characteristics could have been unequally distributed between regions and countries, and therefore a possible explanation for unequal distribution of hospitalizations and secondary care demand in general.

Therefore, our findings may indicate differences in diagnosis and the efficiency of asthma management plans between the regions and countries, and some evidence already confirmed differences in diagnosis of pediatric asthma among regions within Finland.22 Previous research into asthma-related hospital admissions among children identified at least eight preventable factors associated with hospital admission.2 Among those, “failure to use asthma crisis management plan,” and “inappropriate preventive treatment,” ranked as first and third most commonly reported for patients admitted. The “management plan” was only established for 49% of the children, and among those only 9% followed it at the time of need.2 Therefore, it appears that there is room for improvement in terms of appropriate preventive treatment as well as development of individual crisis management plans for patients at the provider side, as well as in terms of patient education. Among other factors, the “low level of asthma knowledge,” partly responsibility of the patients as well as health-care providers, ranked second, and “compliance” ranked fourth. These findings support the notion that pediatric asthma-related hospital admissions are in part a consequence of variations in asthma management at primary care level, which has been previously established for adults.24,7,12 Analyses of small area variations have been successfully used in other disease areas to identify opportunities for improvement in disease management at a population level.2324 For example, Ashton et al25 found substantial geographic variation in the hospital and outpatient use for COPD and seven other chronic diseases in the US Veterans Affairs health-care system.

Several limitations are present in this study. For many reasons, administrative databases routinely include incomplete and biased data that can significantly influence the numerators and denominators used in the analyses. In order to ensure homogeneity of the data sources, our study used the nationwide inpatient registries, which are established in each country included in this article by the ministry of health (government institutes). Due to the nature of the health systems in these countries as well as in Europe in general (“universal” health-care systems), uniform systems of delivery, financing, and tracking of health care within the countries are in place. Therefore, the nature of the data collection within each country is homogeneous, though there may well be differences between the countries. To avoid the latter, four countries were selected that share common history as well as development of the health-care systems within Europe. Data reported from the hospitals to the inpatient registries use the common coding system (ICD). Coding in all four countries is performed by treating physicians on a per-patient/individual basis using a unique patient identifying number. Due to the similarities in the training of medical personnel in Nordic region, we would not expect differential coding between countries, and even less so within the countries. In addition, no financial incentives exist in any of the systems included to code patients differentially (eg, as more severe). Financing in most county councils is based on DRGs, which creates incentives for having systems in place that generate complete and accurate records of hospitalizations. The risk for bias toward more expensive DRGs is low, however, since the salaries of physicians (who record the ICD codes that the DRGs are based on) are not affected by the DRGs. Data quality is periodically checked by the institutes creating inpatient registries, and is reported to be > 99% reliable with respect to diagnoses and patient identification numbers.26

We relied on existing data on hospital resource use that did not have objective outcome measures such as lung function and disease history. Therefore, we could not compare severity of the underlying asthma among different populations. We were only able to establish severity of the current asthma episode. To approximate the latter, we used the ICD coding system. We based our comparisons within and between countries on the assumption that the diagnosis of asthma as a cause of hospital admission through ICD coding is reliable within this geographic area. Since ICD coding is not used for direct billing purposes in Europe as it is in the United States, we would not expect adverse behavior with respect to coding. Even if evidence of such behavior existed, there is no reason to believe it would be adversely distributed, which means substantial differences among the four Nordic countries are not to be expected. Physicians who code patients with respect to ICD system receive salaries independently of the ICD codes reported. Evidence also suggests that when classifying severity, which is based on pathophysiology of the disease as well as medication use,1 patients may be falsely assessed with respect to asthma severity level on the part of physicians. Some of the patients might fall into a higher severity category, based on their underlying pathophysiology, but were well controlled at the time of assessment and were, therefore, “upgraded” to a milder asthma category. This illustrates how assessment of severity level is inextricably confounded with level of control.27 Hence, underlying asthma severity assessment may be problematic in itself. In addition, the specificity of the asthma diagnosis is probably low, particularly in the younger children. This may bias the comparison of hospitalization data among age groups, though the tendency is likely to underdiagnose asthma in young children, which would suggest that the relative burden of asthma hospitalization is even greater in young children. Lack of specificity of diagnosis is unlikely to significantly affect comparisons between regions and countries.

In conclusion, large variations found in this study may indicate significant differences in the efficiency of management plans in the primary and secondary care settings for children with asthma throughout the four Nordic countries. Education and disease management programs may be needed to reduce the variations in hospital resource use and to improve patient care. The measures applied in our study may be used to monitor the effect of such interventions in management plans. It may prove valuable to establish national and international databases to monitor asthma hospitalization rates, readmission rates, and LOS as a tool to evaluate improvements in asthma management.

Abbreviations: DRG = diagnosis related group; ICD = International Classification of Diseases; LOS = length of hospital stay; RHR = relative hazard of readmission

This study was performed at the Department of Pharmacy Practice, Purdue University, West Lafayette, IN.

The study was in part supported by a research grant from Merck & Co., Inc., Whitehouse Station, NJ.

Special thanks to the Danish National Board of Health; Mr. Jakob Lynge Sandegaard, Swedish National Board of Health and Welfare; Mr. Curt-Lennart Spetz, Norwegian Patient Register; Mr. Erik Sverrbo, and the Finnish National Research and Development Centre for Health and Welfare; and Mr. Oleg Nikiforov. We also wish to thank Dr. Mark Messonnier for his contribution toward study design.

Global Initiative for Asthma. Available at http://www.ginasthma.com. Accessed April 1, 2004.
 
Ordonez, G, Phelan, PD, Olinsky, A, et al Preventable factors in hospital admissions for asthma.Arch Dis Child1998;78,143-147. [CrossRef] [PubMed]
 
Hartert, TV, Windom, HH, Peebles, RS, Jr, et al Inadequate outpatients medical therapy for patients with asthma admitted to two urban hospitals.Am J Med1996;100,386-394. [CrossRef] [PubMed]
 
Barnes, PJ, Jonsson, B, Klim, JB The costs of asthma.Eur Respir J1996;9,636-642. [CrossRef] [PubMed]
 
Jacobson, L, Hertzman, P, Lofdahl, CG, et al The economic impact of asthma and chronic obstructive pulmonary disease (COPD) in Sweden in 1980 and 1991.Respir Med2000;94,247-255. [CrossRef] [PubMed]
 
Szucs, TD, Anderhub, H, Rutishauser, M The economic burden of asthma: direct and indirect costs in Switzerland.Eur Respir J1999;13,281-286. [CrossRef] [PubMed]
 
Smith, DH, Malone, DC, Lawson, KA, et al A national estimate of the economic costs of asthma.Am J Respir Crit Care Med1997;156,787-793. [PubMed]
 
Lozano, P, Sullivan, SD, Smith, DH, et al The economic burden of asthma in US children: estimates from the National Medical Expenditure Survey.J Allergy Clin Immunol1999;104,957-963. [CrossRef] [PubMed]
 
Bisgaard, H, Moller, H Changes in risk of hospital readmission among asthmatic children in Denmark, 1978–93.BMJ1999;319,229-230. [CrossRef] [PubMed]
 
Jonasson, G, Lodrup Carlsen, KC, Leegaard, J, et al Trends in hospital admissions for childhood asthma in Oslo, Norway, 1980–95.Allergy2000;55,232-239. [CrossRef] [PubMed]
 
Wennergren, G, Kristjansson, S, Strannegard, IL Decrease in hospitalization for treatment of childhood asthma with increased use of antiinflammatory treatment, despite an increase in prevalence of asthma.J Allergy Clin Immunol1996;97,742-748. [CrossRef] [PubMed]
 
Groban, D, Evans, RM, Edgren, B, et al Clinical benefits and cost reduction associated with a comprehensive asthma management program at a managed care organization.Dis Manag Health Outcomes1998;4,93-100. [CrossRef]
 
Valovirta, E, Kocevar, VS, Kaila, M, et al Inpatient resource utilisation in younger (2–5 yrs) and older (6–14 yrs) asthmatic children in Finland.Eur Respir J2002;20,397-402. [CrossRef] [PubMed]
 
World Health Organization. Available at http://www.who.org. Accessed April 1, 2004.
 
The World Bank. Available at http://www.worldbank.org. Accessed April 1, 2004.
 
Danish Statistical Institute. Available at http://www.dst.dk. Accessed April 1, 2004.
 
Swedish Statistical Institute. Available at http://www.scb.se. Accessed April 1, 2004.
 
National Research and Development Centre for Welfare and Health. Available at http://www.stakes.fi. Accessed April 1, 2004.
 
Nystad, W, Magnus, P, Roksund, O, et al The prevalence of respiratory symptoms and asthma among school children in three different areas of Norway.Pediatr Allergy Immunol1997;8,35-40. [CrossRef] [PubMed]
 
Ronmark, E, Lundback, B, Jonsson, E, et al Asthma, type-1 allergy and related conditions in 7- and 8-year-old children in northern Sweden: prevalence rates and risk factor pattern.Respir Med1998;92,316-324. [CrossRef] [PubMed]
 
Rona, RJ Asthma and poverty.Thorax2000;55,239-244. [CrossRef] [PubMed]
 
Csonka, P, Mertsola, J, Kaila, M, et al Regional variation in the diagnosis of asthma among preschool-age children.Pediatr Allergy Immunol2000;11,189-192. [CrossRef] [PubMed]
 
McPherson, K, Wennberg, JE, Hovind, OB, et al Small-area variations in the use of common surgical procedures: an international comparison of New England, England, and Norway.N Engl J Med1982;307,1310-1131. [CrossRef] [PubMed]
 
Wennberg, JE Understanding geographic variations in health care delivery.N Engl J Med1999;340,52-53. [CrossRef] [PubMed]
 
Ashton, CM, Petersen, NJ, Souchek, J, et al Geographic variations in utilization rates in Veterans Affairs hospitals and clinics.N Engl J Med1999;340,32-39. [CrossRef] [PubMed]
 
“Patientregistret: Utskrivningar från sluten vård 1964–2001. Kvalitet och innehåll” Epidemiologiskt Centrum, Socialstyrelsen (National Board on Health and Welfare), February 2003. Available at http://www.sos.se. Accessed April 1, 2004.
 
Vollmer, WM, Markson, LE, O’Connor, E, et al Association of asthma control with health care utilization and quality of life.Am J Respir Crit Care Med1999;160,1647-1652. [PubMed]
 

Figures

Tables

References

Global Initiative for Asthma. Available at http://www.ginasthma.com. Accessed April 1, 2004.
 
Ordonez, G, Phelan, PD, Olinsky, A, et al Preventable factors in hospital admissions for asthma.Arch Dis Child1998;78,143-147. [CrossRef] [PubMed]
 
Hartert, TV, Windom, HH, Peebles, RS, Jr, et al Inadequate outpatients medical therapy for patients with asthma admitted to two urban hospitals.Am J Med1996;100,386-394. [CrossRef] [PubMed]
 
Barnes, PJ, Jonsson, B, Klim, JB The costs of asthma.Eur Respir J1996;9,636-642. [CrossRef] [PubMed]
 
Jacobson, L, Hertzman, P, Lofdahl, CG, et al The economic impact of asthma and chronic obstructive pulmonary disease (COPD) in Sweden in 1980 and 1991.Respir Med2000;94,247-255. [CrossRef] [PubMed]
 
Szucs, TD, Anderhub, H, Rutishauser, M The economic burden of asthma: direct and indirect costs in Switzerland.Eur Respir J1999;13,281-286. [CrossRef] [PubMed]
 
Smith, DH, Malone, DC, Lawson, KA, et al A national estimate of the economic costs of asthma.Am J Respir Crit Care Med1997;156,787-793. [PubMed]
 
Lozano, P, Sullivan, SD, Smith, DH, et al The economic burden of asthma in US children: estimates from the National Medical Expenditure Survey.J Allergy Clin Immunol1999;104,957-963. [CrossRef] [PubMed]
 
Bisgaard, H, Moller, H Changes in risk of hospital readmission among asthmatic children in Denmark, 1978–93.BMJ1999;319,229-230. [CrossRef] [PubMed]
 
Jonasson, G, Lodrup Carlsen, KC, Leegaard, J, et al Trends in hospital admissions for childhood asthma in Oslo, Norway, 1980–95.Allergy2000;55,232-239. [CrossRef] [PubMed]
 
Wennergren, G, Kristjansson, S, Strannegard, IL Decrease in hospitalization for treatment of childhood asthma with increased use of antiinflammatory treatment, despite an increase in prevalence of asthma.J Allergy Clin Immunol1996;97,742-748. [CrossRef] [PubMed]
 
Groban, D, Evans, RM, Edgren, B, et al Clinical benefits and cost reduction associated with a comprehensive asthma management program at a managed care organization.Dis Manag Health Outcomes1998;4,93-100. [CrossRef]
 
Valovirta, E, Kocevar, VS, Kaila, M, et al Inpatient resource utilisation in younger (2–5 yrs) and older (6–14 yrs) asthmatic children in Finland.Eur Respir J2002;20,397-402. [CrossRef] [PubMed]
 
World Health Organization. Available at http://www.who.org. Accessed April 1, 2004.
 
The World Bank. Available at http://www.worldbank.org. Accessed April 1, 2004.
 
Danish Statistical Institute. Available at http://www.dst.dk. Accessed April 1, 2004.
 
Swedish Statistical Institute. Available at http://www.scb.se. Accessed April 1, 2004.
 
National Research and Development Centre for Welfare and Health. Available at http://www.stakes.fi. Accessed April 1, 2004.
 
Nystad, W, Magnus, P, Roksund, O, et al The prevalence of respiratory symptoms and asthma among school children in three different areas of Norway.Pediatr Allergy Immunol1997;8,35-40. [CrossRef] [PubMed]
 
Ronmark, E, Lundback, B, Jonsson, E, et al Asthma, type-1 allergy and related conditions in 7- and 8-year-old children in northern Sweden: prevalence rates and risk factor pattern.Respir Med1998;92,316-324. [CrossRef] [PubMed]
 
Rona, RJ Asthma and poverty.Thorax2000;55,239-244. [CrossRef] [PubMed]
 
Csonka, P, Mertsola, J, Kaila, M, et al Regional variation in the diagnosis of asthma among preschool-age children.Pediatr Allergy Immunol2000;11,189-192. [CrossRef] [PubMed]
 
McPherson, K, Wennberg, JE, Hovind, OB, et al Small-area variations in the use of common surgical procedures: an international comparison of New England, England, and Norway.N Engl J Med1982;307,1310-1131. [CrossRef] [PubMed]
 
Wennberg, JE Understanding geographic variations in health care delivery.N Engl J Med1999;340,52-53. [CrossRef] [PubMed]
 
Ashton, CM, Petersen, NJ, Souchek, J, et al Geographic variations in utilization rates in Veterans Affairs hospitals and clinics.N Engl J Med1999;340,32-39. [CrossRef] [PubMed]
 
“Patientregistret: Utskrivningar från sluten vård 1964–2001. Kvalitet och innehåll” Epidemiologiskt Centrum, Socialstyrelsen (National Board on Health and Welfare), February 2003. Available at http://www.sos.se. Accessed April 1, 2004.
 
Vollmer, WM, Markson, LE, O’Connor, E, et al Association of asthma control with health care utilization and quality of life.Am J Respir Crit Care Med1999;160,1647-1652. [PubMed]
 
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