Download the impact of asthma on the patient, the family

REVIEW
THE IMPACT OF ASTHMA ON THE PATIENT,
THE FAMILY, AND SOCIETY
—
Erwin W. Gelfand, MD*
ABSTRACT
This article discusses the impact of asthma on
the patient, the family, and society and considers
the role of primary care providers and pediatricians in reducing the burden of asthma. Nearly
8% of the US population suffers from asthma. The
most recent government data show that asthmaattack prevalence, defined as the proportion of
individuals with at least 1 asthma episode in a
12-month period (a crude gauge of the number
of individuals who have uncontrolled asthma and
are therefore at risk for poor outcomes), was
4.2%. Consistent with its chronicity and its manifestations, including pulmonary function impairment and symptoms of wheezing, cough,
dyspnea, and chest tightness, asthma impairs
patients’ well-being and can significantly interfere with the ability to undertake normal daily
activities. Among those with at least 1 asthma
attack in the previous year in the 2002 National
Health Interview Survey, asthma was responsible
for 14.7 million missed school days in children 5
to 17 years old and 11.8 million missed workdays in adults 18 years and older. In keeping
with the high prevalence and life impact of asthma, asthma-associated healthcare resource use is
substantial. In 2002, asthma was responsible for
13.9 million outpatient visits, 1.9 million emergency department visits, and 484 000 hospitalizations in the United States. The annual
economic cost of asthma in the United States is
estimated at $14 billion. Children are disproportionately affected by asthma and have higher
*Chairman, Department of Pediatrics, National Jewish
Medical and Research Center, Denver, Colorado.
Address correspondence to: Erwin W. Gelfand, MD,
Chairman, Department of Pediatrics, National Jewish
Medical and Research Center, 1400 Jackson Street,
Denver, CO 80206. E-mail: [email protected].
Johns Hopkins Advanced Studies in Medicine
■
rates of asthma-associated healthcare use and
greater asthma-related activity limitation than
adults. These data reflect a growing burden of
asthma in terms of morbidity, quality of life, and
healthcare costs and demonstrate that asthma
care is falling short of National Heart, Lung, and
Blood Institute goals. Primary care providers,
including pediatricians, play a pivotal role in
improving quality of care for asthma given that
most cases of asthma are diagnosed and managed in the primary care setting. Evidence suggests that primary care providers’ adherence to
national guidelines for asthma care can contribute significantly to reducing the burden of
asthma.
(Adv Stud Med. 2008;8(3):57-63)
A
s stated, nearly 8% of the US population suffers from asthma,1 and for
many of these patients, asthma is poorly controlled, despite advances in
knowledge about asthma pathophysiology and the availability of effective therapy.2,3 Data
reflecting the growing burden of asthma in terms of
morbidity, quality of life, and healthcare costs demonstrate that asthma care is falling short of National
Heart, Lung, and Blood Institute (NHLBI) goals,
which include prevention of chronic and troublesome
symptoms, maintenance of near-normal pulmonary
function and normal activity levels, and prevention of
recurrent exacerbations requiring emergency-department visits or hospitalization.1,4 This article discusses
the impact of asthma on the patient, the family, and
society and considers the role of primary care
providers and pediatricians—who are consulted by
the majority of patients who have asthma—in reducing the burden of asthma.
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REVIEW
least 35 years old (2.4%; Figure 2). Among females,
asthma-attack prevalence did not significantly vary by
age (4.4% in patients 0–14 years old; 5.5% in those
15–34 years old; 4.9% in those at least 35 years old;
Figure 2). Sex-adjusted asthma-attack prevalence rates
were highest among non-Hispanic/non-Latino blacks
0 to 14 years old (6.2%) followed by Hispanics or
PREVALENCE OF ASTHMA
58
Figure 1. Prevalence of Current Asthma in the United
States, January to September 2005
12
10.7
Percentage
10
8
9.0
9.6
9.1
7.7
7.5
7.4
9.3
7.3
6.3
6
5.2
Total
5.0
Male
4
Female
2
Any age
0–4 years
15–34 years
35 years
and older
Data from National Asthma Education and Prevention Program.1
Figure 2. Asthma-Attack Prevalence*
8
6.8
7
6
Percentage
The prevalence of asthma has increased both in the
United States and globally during the past 4 decades.5
The most comprehensive data on asthma prevalence in
the United States come from the National Health
Interview Survey (NHIS), an ongoing US populationbased disease-surveillance study conducted by the US
Centers for Disease Control and Prevention National
Center for Health Statistics. NHIS data are drawn
from household interviews of a nationally representative sample of the civilian noninstitutionalized population. Information on asthma status in the NHIS was
self-reported by individuals ages 18 years or older or
collected from an adult family member for children
younger than 18 years old. Data from the NHIS survey
conducted from January to September 2005, the most
recent time period for which data are available, show
that 7.7% of individuals of any age in the United States
currently have asthma (Figure 1).1 This prevalence rate
exceeds that in the 2 preceding years (2003, 7.1%;
2004, 7.3%). Among males, asthma prevalence was
approximately twice as high in those 14 years old or
younger (10.7%) than in patients 15 to 34 years old
(5.2%) or those at least 35 years old (5.0%; Figure 1).
Among females, asthma prevalence did not significantly vary by age (7.5% in patients 0–14 years old; 9.6%
in patients 15–34 years old; 9.3% in those at least 35
years old; Figure 1). Sex-adjusted asthma prevalence
was highest among non-Hispanic/non-Latino blacks 0
to 14 years old (12.8%) followed by Hispanics or
Latinos 0 to 14 years old (9.5%), blacks 15 years old or
older (8.4%), whites 0 to 14 years old (7.8%), whites
15 years old and older (7.5%), and Hispanics or
Latinos 15 years older or older (5.3%).
A similar pattern of results was found for asthmaattack prevalence, defined as the proportion of individuals with at least 1 asthma episode during the 12
months before the survey.1 Asthma-attack prevalence
provides a crude gauge of the number of individuals
who have uncontrolled asthma and are therefore at risk
for poor outcomes, such as hospitalization. Overall,
4.2% of individuals of any age experienced at least 1
asthma episode during the 12 months before the survey (Figure 2).1 This rate slightly exceeds that in the 2
preceding years (2003, 3.9%; 2004, 4.1%). Among
males, asthma-attack prevalence was more than 2
times higher in those 14 years old or younger (6.8%)
than in patients 15 to 34 years old (2.6%) or those at
5.6
4.9
4.4
4.2
4
5.5
5.0
5
4.0
3.7
3.4
3
2.6
Total
Male
2.4
Female
2
1
Any age
0–14 years
15–34 years
35 years
and older
*Percentage of persons in the United States with at least 1 asthma episode during the 12 months before the National Health Interview Survey conducted from
January to September 2005.
Data from National Asthma Education and Prevention Program.1
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March 2008
REVIEW
Latinos 0 to 14 years old (5.7%), whites 0 to 14 years
old (5.2%), whites 15 years old and older (3.9%),
blacks 15 years old and older (3.8%), and Hispanics or
Latinos 15 years old or older (3.1%).
IMPACT OF ASTHMA ON THE PATIENT AND THE FAMILY
ASTHMA-ASSOCIATED HEALTHCARE RESOURCE USE
In keeping with the high prevalence and life impact
of asthma, asthma-associated healthcare resource use is
substantial. Data on healthcare resource use attributed
to asthma come from the US Centers for Disease
Control and Prevention National Ambulatory Medical
Care Survey, a nationally representative survey on the
Consistent with its chronicity and its manifestations, including pulmonary-function
impairment and symptoms of wheezing,
cough, dyspnea, and chest tightness, asthma impairs patients’ well-being and can
Table 1. Selected Chronic Health Conditions Causing Limitation of
significantly interfere with the ability to
Activity Among Children, United States, 2003–2004
undertake normal daily activities. Among
those with at least 1 asthma attack in the
Younger than
previous year in the 2002 NHIS, asthma
5 Years
5–11 Years
12–17 Years
was responsible for 14.7 million missed
Number of children with activity limitation per 1000 population
school days in children 5 to 17 years old
Speech problem
10.4
29.0
5.2
and 11.8 million missed workdays in
2
adults 18 years and older. These data do
Asthma/breathing problem
7.2
6.8
5.7
not take into account the larger burden of
presenteeism (ie, showing up for work but
Mental retardation/other
being unable to perform to standards). In
7.5
10.8
9.8
developmental problem
2003 to 2004, limitation of activity
Other mental, emotional,
because of chronic health conditions was
behavioral problem
3.4
13.1
15.4
reported for 7% of children younger than
18 years in the United States.1 Among
Attention-deficit/
preschool children, asthma was a leading
hyperactivity disorder
1.9
18.7
21.9
cause of activity limitation. Only speech
Learning disability
2.7
19.6
29.1
problems and mental retardation were
Data
from
National
Asthma
Education
and
Prevention
Program.
associated with greater activity limitation
than asthma in this age group (Table 1).1
Asthma also affects the lives of family
Table 2. Asthma-Related Healthcare Resource Use in the United
members who provide care for patients
States, 2002
with asthma. In a study of children with
persistent asthma and their caregivers,
Emergencyapproximately 33% of caregivers missed
Outpatient Visits
Department Visits
Hospitalizations
work during the 12-month study because
Total
492
67
17
of their child’s asthma.6 The amount of
Sex
work lost was strongly and negatively corFemale
585
69
19
related with the degree of asthma control
Male
384
65
14
as assessed by use of rescue medication,
Race
nocturnal symptoms, impairment of
Black
482
217
36
activities, and asthma crises. Caregivers of
White
493
45
11
children with poorly controlled asthma
Age
were 8 times more likely to lose more than
18 years old
181
24
13
5 days of work during the study period
0–17 years
687
100
27
than caregivers of children with wellData are expressed as units per 10 000 population.
Data from US Centers for Disease Control and Prevention.
controlled asthma.
1
≥
2
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use of ambulatory medical care services in the United
States, and the National Hospital Discharge Survey, a
national probability survey on characteristics of
patients discharged from nonfederal, short-stay hospitals in the United States. The following statistics were
compiled for 2002, the most recent year for which
published data are available (Table 2).2
• Asthma was the reason for 13.9 million outpatient visits, or 492 outpatient visits per 10 000
people. The frequency of outpatient visits among
children ages 0 to 17 years (687 per 10 000 individuals) substantially exceeded that among
adults 18 years and older (181 per 10 000 individuals). The number of asthma-related outpatient visits per 10 000 people was higher in
females (585) than males (384) and was similar
between blacks (482) and whites (493). (Data on
healthcare resource use among Hispanics were
not reported in the 2002 summary.)
• Asthma was responsible for 1.9 million emergency department visits, or 67 per 10 000 people. The frequency of emergency department
visits among children ages 0 to 17 years (100 per
10 000 individuals) substantially exceeded that
among adults 18 years and older (24 per 10 000
individuals). Emergency department visits were
particularly frequent among children ages 0 to 4
years (162 per 10 000). The number of asthmarelated emergency department visits per 10 000
people was similar between females (69) and
males (65) and higher in blacks (217) than
whites (45).
• Asthma was the reason for 484 000 hospitalizations, or 17 per 10 000 people. The frequency
of asthma-related hospitalizations among children ages 0 to 17 years (27 per 10 000 individuals) substantially exceeded that among adults
18 years and older (13 per 10 000 individuals).
Asthma-related hospitalizations were particularly frequent among children ages 0 to 4 years (59
per 10 000). The number of asthma-related hospitalizations per 10 000 people was similar
between females (19) and males (14) and higher in blacks (36) than whites (11).
The annual economic cost of asthma in the United
States is estimated at $14 billion, a value that includes
both direct and indirect costs.8 Direct costs, or those
associated with the delivery of healthcare, include components such as the cost of medications, hospitalizations, emergency department visits, office visits, and
medical tests and procedures. Indirect costs are those
associated with illness-attributed lost or reduced productivity. Data from a cross-sectional survey of 401
adults with asthma drawn from a random samples of
northern California pulmonologists, allergist-immunologists, and family practitioners suggest that lost
workplace productivity and pharmaceuticals account
for the majority of the economic costs of asthma.9 The
total average annual cost of asthma per person was
$4912, of which 65% ($3180) was direct costs and
35% ($1732) was indirect costs. The main components
of direct costs included pharmaceuticals ($1605 per
person per year), hospital admissions ($463), and nonemergency department ambulatory visits ($342). The
main components of indirect costs included cessation
of work ($1062 per person per year) and loss of workdays among those remaining employed ($486). The
costs attributed to presenteeism may far exceed those
due to loss of workdays.10 Self-reported disease severity
was strongly and directly related to total annual perperson costs, which were $2646, $4530, and $12 813
for mild, moderate, and severe asthma, respectively.
ASTHMA MORTALITY
CHILDHOOD ASTHMA
Asthma mortality has increased in the past 2 decades
in western countries, including the United States. In
The epidemiologic and outcomes data described
earlier in the article suggest that children are dispro-
60
2002, the most recent year for which US mortality statistics were published, asthma was the cause of 1.5 per
100 000 deaths in the United States (0.3 per 100 000 in
children ages 0–17 years and 1.9 per 100 000 in adults
ages 18 years and older).2 Deaths due to asthma per 100
000 individuals were more frequent among females
(1.7) than males (1.2), and among non-Hispanic blacks
(3.7) than Hispanics (1.4) or non-Hispanic whites
(1.2). The higher death rate in non-Hispanic blacks
than in other ethnic groups in the United States has
been attributed to several factors, including lack of
access to healthcare, more severe asthma, genetic determinants, and higher prevalence of asthma.7
ECONOMIC COST OF ASTHMA
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portionately affected by asthma.11 In fact, asthma is the
most common chronic disease of childhood and the
leading cause of hospitalizations in children.9,12 The
peak incidence of asthma occurs during the first year
of life, and 8 of 10 children who develop asthma experience their first episode of wheezing before their third
birthday.13-15 The onset of more than 80% of cases of
persistent asthma is estimated to occur before the age
of 6 years.16 Difficult to distinguish from other respiratory conditions and challenging to manage in the very
young patient, childhood asthma is underdiagnosed
and undertreated.12 Poorly controlled asthma is particularly of concern in the growing child because it may
impact emotional, intellectual, and physical development (eg, restricting children’s activities, such as running, walking, and vocalizing, impairing children’s
emotional health, and causing children to miss school
or other intellectual or social activities).13,16-18 Poorly
controlled asthma in childhood is also of concern
because it may lead to more rapid progression of disease and deterioration of pulmonary function than
well-controlled asthma.13
ASTHMA PATHOPHYSIOLOGY
Conversely, good control of childhood asthma
may prevent or mitigate the development of more
serious asthma or irreversible airway obstruction later
in life.19 Recent advances in understanding of asthma
pathophysiology suggest the importance of achieving
good asthma control early in the course of the disease.
Asthma is manifested by chronic airway inflammation
leading to bronchial hyperresponsiveness with symptoms, including wheezing, cough, dyspnea, and a feeling of tightness in the chest.20 The inflammation is
caused by myriad cells (eg, mast cells, neutrophils,
eosinophils, and macrophages) and mediators (eg,
cytokines, chemokines, histamine, leukotrienes,
thromboxanes, and reactive oxygen species), the relative contributions of which to asthma pathogenesis
may vary depending on patient- and context-specific
factors.21 Contradicting the historical conception of
all forms of asthma as reversible, recent evidence suggests that asthma is associated with airway remodeling
or permanent structural changes, including subbasement membrane fibrosis, smooth muscle hyperplasia,
angiogenesis, and glandular hyperplasia.21 Although
the clinical significance of airway remodeling has not
been established,22,23 airway remodeling may con-
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tribute to progression of asthma and could lead to
progressive loss of lung function. The structural
changes that characterize airway remodeling have
been identified in mild and moderate asthma as well
as severe fatal asthma.21
Asthma appears to involve repetitive cycles of exacerbation and remission with underlying persistent or
chronic inflammation. This pathology results in structural changes to the airways that over time can become
permanent (airway remodeling). Although some evidence, reviewed in more detail by Drs Schleimer and
Patel in this monograph, suggests that early initiation
of anti-inflammatory therapy for asthma can retard or
prevent the loss of lung function or the progression to
irreversible structural changes in the airways and airway remodeling, other data suggest otherwise—studies
in children treated with steroids have shown little to
no disease modifying effects of corticosteroids even
when begun early in infancy/childhood.24-26
Nevertheless, because of benefits in reducing symptoms, exacerbations, and the need for rescue medications, anti-inflammatory therapy with inhaled
corticosteroids is recommended as a cornerstone of
asthma therapy at all levels of disease severity in current treatment guidelines.4
Advances in the genetics and genomics of asthma,
an area of active research, offers the potential for better understanding of asthma pathophysiology and
improvement in therapy.27 Several genes and chromosomal regions linked to asthma and related respiratory
diseases have been identified.28 Likewise, gene loci that
modify the atopic response as well as nonspecific
inflammation and airway reactivity have been found.
Polymorphisms in the gene for the β2 adrenergic
receptor may determine response and account for
adverse effects of β agonist therapy in patients with
asthma.8 Genetic and genomic research thus might
help improve the ability to target asthma therapy and
maximize the institution of the most appropriate therapy in the individual patient.
CONCLUSIONS
Notwithstanding advances during recent decades
in the basic science of asthma and its treatments, the
detrimental humanistic and economic consequences
of asthma remain substantial. The guidelines by the
National Asthma Education and Prevention Program
(NAEPP) for the diagnosis and management of asth-
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ma were developed to help improve asthma care,
decrease asthma-associated morbidity and mortality,
and reduce the economic and societal burdens of asthma.4 The 2007 revised guidelines include new material
emphasizing the importance of vigilant asthma control
as well as new information on aspects of asthma management, including treating childhood asthma, controlling environmental factors that can cause asthma
symptoms, selecting pharmacotherapy, and educating
patients. Although the guidelines have been in place for
several years and have been widely disseminated and
publicized, they have not been effectively implemented
in many healthcare settings. Moreover, NHLBI goals of
asthma care—prevention of symptoms and exacerbations; maintenance of normal pulmonary function and
activity levels; provision of well-tolerated, effective
pharmacotherapy; minimization of the need for emergency department visits or hospitalizations; and achieving patients’ expectations of asthma care—have not
been met for many patients with asthma.2,3
The failure to achieve the NHLBI goals of asthma
care in many patients is illustrated by results of a
nationally representative survey conducted after publication of the guidelines and administered to 2509
patients with asthma or parents of children with asthma.3 Thirty-one percent (31%) of patients with asthma
indicated that the disease limits their lifestyle, and 45%
said that they cannot do things they would like to do
because of asthma. Activity limitations were reported
by 64% of adults with asthma compared to 26% of a
national cross-sectional sample of 1000 adults in the
general public. Approximately 33% of patients with
asthma (30%) reported being awakened at night
because of breathing problems at least once a week. Use
of rescue inhalers at least once daily was reported by
25% of patients with mild intermittent asthma, 33%
with mild persistent asthma, 53% with moderate persistent asthma, and 73% with severe persistent asthma.
Primary care providers, including pediatricians, can
play a pivotal role in improving quality of care for
asthma in the United States given that most cases of
asthma are diagnosed and managed in the primary
care setting.5 Evidence suggests that primary care
providers’ adherence to NAEPP guidelines for asthma
care can contribute significantly to reducing the burden of asthma.29,30 For example, a citywide diseasemanagement program designed to increase primary
care providers’ adherence to NAEPP guidelines was
found to reduce healthcare resource use among a
62
cohort of 3748 children with asthma in a study conducted in Hartford, Connecticut.30 After primary care
providers’ enrollment in the disease-management program, paid claims for inhaled corticosteroids increased
by 25%, and provider adherence to the guidelines
increased to 96% from a pre-enrollment baseline of
38%. These trends coincided with a 35% decrease in
hospitalizations, a 27% decrease in emergency department visits, and a 19% decrease in outpatient visits
among children with asthma whose providers participated in the program. Improvement in asthma outcomes is thus achievable. Primary care providers, who
constitute the front line of asthma care, and pediatricians, who provide care for the segment of the population most affected by asthma, can effect positive results
by implementing asthma guidelines and keeping
abreast of the most current findings in asthma pathophysiology and advances in therapy.
REFERENCES
1. National Asthma Education and Prevention Program.
Guidelines for the Diagnosis and Management of Asthma.
Bethesda, MD: US Department of Health and Human Services,
National Institutes of Health; 2007. NIH publication 07-4051.
2. US Centers for Disease Control and Prevention. Asthma
prevalence, healthcare use, and mortality, 2002. Available
at: http://www.cdc.gov/nchs/products/pubs/pubd/hestats/asthma/asthma.htm. Accessed January 5, 2007.
3. The state of asthma in American: two landmark surveys.
Available at: www.asthmainamerica.com. Accessed January
9, 2007.
4. National Asthma Education and Prevention Program.
Guidelines for the Diagnosis and Management of Asthma.
Bethesda, MD: US Department of Health and Human Services,
National Institutes of Health; NIH Publication 97-4051.
5. Braman SS. The global burden of asthma. Chest.
2006;130:4S-12S.
6. Laforest L, Yin D, Kocevar VS, et al. Association between
asthma control in children and loss of workdays by caregivers. Ann Allergy Asthma Immunol. 2004;93:265-271.
7. Lugogo NL, Kraft M. Epidemiology of asthma. Clin Chest
Med. 2006;27:1-15.
8. O’Connell EJ. The burden of atopy and asthma in children.
Allergy. 2004;39(suppl 78):7-11.
9. Cisternas MG, Blanc PD, Yen IH, et al. A comprehensive
study of the direct and indirect costs of adult asthma. J Allergy
Clin Immunol. 2003;111:1212-1218.
10. Gelfand EW, Colice GL, Fromer L, et al. Use of the health
plan employer data and information set for measuring and
improving the quality of asthma care. Ann Allergy Asthma
Immunol. 2006;97:298-305.
11. Castro HJ, Malka-Rais J, Bellanti JA. Current epidemiology of
asthma: emerging patterns of asthma. Allergy Asthma Proc.
2005;26:79-82.
12. Szefler SJ. Challenges in assessing outcomes for pediatric
asthma. J Allergy Clin Immunol. 2001;105:S456-S464.
Vol. 8, No. 3
■
March 2008
REVIEW
13. Weiss ST. Epidemiology and heterogeneity of asthma. Ann
Allergy Asthma Immunol. 2001;87(suppl):5-8.
14. Wright AL, Taussig LM. Lessons from long-term cohort studies.
Eur Respir J. 1998;12(suppl 27):17s-22s.
15. Martinez FD. Definition of pediatric asthma and associated
risk factors. Pediatr Pulmonol Suppl. 1997;15:9-12.
16. Lowe L, Custovic A, Woodcock A. Childhood asthma. Curr
Allergy Asthma Rep. 2004;4:159-165.
17. Reichenberg K, Broberg AG. Quality of life in childhood
asthma: use of the Paediatric Asthma Quality of Life
Questionnaire in a Swedish Sample of children 7 to 9 years
old. Acta Paediatr. 2000;89:989-995.
18. Asmussen L, Olson LM, Grant EN, et al. Reliability and validity of the Children’s Health Survey for Asthma. Pediatrics.
1999;104:e71.
19. The Childhood Asthma Management Program Research
Group. Long-term effects of budesonide or nedocromil in children with asthma. N Engl J Med. 2000;343:1054-1063.
20. Canonica GW. Treating asthma as an inflammatory disease.
Chest. 2006;130:21S-28S.
21. Jarjour NN, Kelly EAB. Pathogenesis of asthma. Med Clin N
Am. 2002;86:925-936.
22. Bergeron C, Boulet LP. Structural changes in airway diseases:
characteristics, mechanisms, consequences, and pharmacologic modulation. Chest. 2006;129:1068-1087.
Johns Hopkins Advanced Studies in Medicine
■
23. Lazarus SC. Mild persistent asthma: is any treatment needed? J Allergy Clin Immunol. 2006;118:805-808.
24. Guilbert TW, Morgan WJ, Zeiger RS, et al. Long-term
inhaled corticosteroids in preschool children at high risk for
asthma. N Engl J Med. 2006;354:1985-1997.
25. Bisgaard H, Hermansen MN, Loland L, et al. Intermittent
inhaled corticosteroids in infants with episodic wheezing. N
Engl J Med. 2006;354:1998-2005.
26. Murray CS, Woodcock A, Langley SJ, et al. Secondary prevention of asthma by the use of Inhaled Fluticasone propionate in Wheezy INfants (IFWIN): double-blind,
randomised, controlled study. Lancet. 2006;368:754-762.
27. Harrison TA, Burke W, Edwards KL. The asthma consultative
process: a collaborative approach to integrating genomics
into public health practice. Prev Chronic Dis. 2005;2:A27.
28. Cookson W. Genetics and genomics of asthma and allergic
diseases. Immunol Rev. 2002;190:195-206.
29. Cloutier MM, Hall CB, Wakefield DB, et al. Use of asthma
guidelines by primary care providers to reduce hospitalizations and emergency department visits in poor, minority,
urban children. J Pediatr. 2005;146:591-597.
30. Carlton BG, Lucas DO, Ellis EF, et al. The status of asthma
control and asthma prescribing practices in the United States:
results of a large prospective asthma control survey of primary care practices. J Asthma. 2005;42:529-535.
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