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Impact of Low Birth Weight on Early Childhood Asthma in the United States
Ann-Marie Brooks, MD;
Robert S. Byrd, MD, MPH;
Michael Weitzman, MD;
Peggy Auinger, MS;
John T. McBride, MD
Arch Pediatr Adolesc Med. 2001;155:401-406.
ABSTRACT
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Objective To estimate the independent contribution of birth weight to asthma prevalence
among children younger than 4 years in the United States and to compare the
magnitude of its effect on asthma between African American and white children.
Design Cross-sectional analysis using the 1988 National Maternal-Infant Health
Survey and 1991 Longitudinal Follow-up Survey.
Setting United States.
Patients Eight thousand seventy-one subjects, selected from a randomized, systematic
population-based sample and weighted to be nationally representative, who
completed both initial and longitudinal follow-up surveys and reported information
on asthma diagnosis.
Main Outcome Measures Birth weight and other sociodemographic factors linked to birth outcome
were analyzed for independent association with physician-diagnosed asthma
by age 3 years.
Results The prevalence of asthma varied by birth weight category: 6.7% in children
2500 g or more at birth, 10.9% in children 1500 to 2499 g at birth, and 21.9%
in children less than 1500 g at birth (very low birth weight [VLBW]) (P<.001). Some of the characteristics shown to be independently
associated with asthma included: VLBW (odds ratio [OR], 2.9; 95% confidence
interval [CI], 2.3-3.6), moderately low birth weight (OR, 1.4; 95% CI, 1.1-1.8),
and African American race (OR, 1.9; 95% CI, 1.6-2.4). In stratified analyses,
the independent association between VLBW and asthma in white and African American
populations was: ORwhite, 3.1 (95% CI, 2.2-4.3) and ORAfrican
American, 2.5 (95% CI, 2.0-3.3). The prevalence of VLBW, however, was
tripled in African American compared with white children (1.8% vs 0.6%).
Conclusions These data confirm findings of other studies that identify a strong
independent association between low birth weight and asthma. For this 1988
national birth cohort, an estimated 4000 excess asthma cases were attributable
to birth weight less than 2500 g. Although the strength of the independent
association between VLBW and asthma was smaller in the African American population,
the substantially increased prevalence of VLBW in this community may contribute
to the disproportionately increased prevalence of asthma among African American
children.
INTRODUCTION
THE BURDEN of asthma in very young children has increased markedly in
this country during the past 2 decades. In children 0 to 4 years old, asthma
prevalence has risen 164% (from 2.2% in 1980 to 5.8% in 1994).1
Similarly, the cost of asthma-related health care is disproportionately higher
in very young children compared with other age categories. Although children
4 years or younger represent less than 30% of the pediatric asthma population
nationally, they account for nearly 50% of total direct asthma costs.2 Identifying individual risk factors that contribute
to the burden of asthma in this age group is useful for generating pathophysiologic
hypotheses for these disturbing trends and for directing public health resources.
Although many small studies have demonstrated an association between
low birth weight (LBW) and asthma throughout childhood,3, 4, 5, 6, 7
to our knowledge, none have described the extent to which LBW contributes
to the "epidemic" of asthma in very young children. On the individual level,
the effects of LBW on lung function and respiratory health appear to be most
pronounced in the first few years of life.8, 9, 10
The impact of LBW on asthma prevalence, therefore, may be most noticeable
in early childhood. Nationally, the prevalence of both LBW11
and asthma1 has been increasing during the
past 2 decades. There has also been a significant increase in the use of neonatal
respiratory support modalities,12 which may
contribute to disturbances in pulmonary function. These points suggest that
LBW may have a role in the trends of increasing asthma burden in early childhood
asthma.
Understanding differential trends in LBW may also help to explain some
of the disparity in asthma burden between white and African American children.
African American children have a greater risk for asthma and frequent wheeze
than white children.13 Low birth weight is
also more prevalent in African American populations.11
The increased numbers of children with LBW may simply translate to an increased
contribution of LBW to asthma prevalence in the African American population.
Pulmonary development and/or physiologic responses to perinatal respiratory
interventions appears to differ between races because African American race
is associated with decreased risk for oxygen dependence and chronic lung disease
(CLD), even after gestational age and birth weight are controlled for.14, 15, 16 The independent association
between LBW and asthma, therefore, is not necessarily the same between African
American and white populations.
This article describes the contribution of LBW to early childhood asthma
prevalence. We used a nationally representative sample to estimate the strength
of the association between LBW and asthma (relative risk) as well as the magnitude
of population-wide impact of LBW on the number of children with asthma (attributable
risk). Our objective was to test the hypothesis that LBW is independently
associated with asthma development by the fourth year of life and that this
association significantly affects asthma prevalence in the general population.
We also assessed the association between prenatal risk factors, including
LBW, and asthma in African American and white children. Our objective was
to identify differences in prenatal exposures that could help to explain the
disparity of early childhood asthma burden between these 2 populations.
METHODS
Data from the 1988 National Maternal-Infant Health Survey (NMIHS) and
the 1991 Longitudinal Follow-up Survey were analyzed for this study. The NMIHS
was conducted by the National Center for Health Statistics and represents
a randomized, systematic sample drawn from civilian, noninstitutionalized
vital records in the United States and the District of Columbia. African American
and LBW infants were oversampled, so that the final sample composition was
approximately 50% African American and 30% LBW infants. All data were subsequently
weighted to be nationally representative. The child's primary caretaker, in
most cases the mother, was questioned. The sample of caretakers contacted
totaled 13 417; 74% returned the original questionnaire. The initial
survey contained sociodemographic information, prenatal history, and delivery
outcomes.
Caretakers responding to the first survey were recontacted in their
child's third year of life for the Longitudinal Follow-up Survey. The longitudinal
follow-up included all women who completed the baseline survey (except for
those who said they did not want to be recontacted) and whose child was alive
in 1991. There was an 88% completion rate. Of the 8145 subjects who completed
the longitudinal survey, 8071 answered the question on physician-diagnosed
asthma and were included in this analysis. The follow-up survey questioned
caretakers on the child's developmental, medical, and social history during
the 3 years since birth. Although abstracted information from clinician and
hospital medical records were included in the original data set, this information
was not included in the analyses reported in this article because a substantial
amount of data was missing.
Independent variables included potential confounders of the relationship
between LBW and asthma available from the NMIHS, such as sex of the child,13, 17, 18, 19, 20
maternal age at the child's birth,13, 17, 21, 22, 23
race,7, 13, 22, 24
maternal education and socioeconomic status,7, 13, 18, 22, 24, 25, 26
extent of prenatal care and maternal weight gain,27
and history of maternal smoking of tobacco products before, after, and/or
during the pregnancy.6, 17, 18, 20, 26
A poverty status variable was developed by means of report of family income
and number of members in the household and categorized according to standard
national poverty levels. Birth weight, extracted from the child's birth certificate,
also was obtained from the NMIHS. Standard limits for moderately low birth
weight (MLBW) (1500-2499 g) and very low birth weight (VLBW) (<1500 g)
were used to categorize children. Racial categories in the NMIHS included
white, African American, and other. A final variable in the analysis, history
of CLD, was identified in the Longitudinal Follow-up Survey by the question:
" . . . have [you] ever been told by a doctor, nurse, or other health care
provider that [child's name] has any other chronic respiratory, lung, or breathing
condition?" In the child with LBW, this question could be expected to identify
those with a history of CLD of prematurity.
The sole outcome measure in this study was physician-diagnosed asthma
in the first 3 years of life. Children were categorized as having asthma if
there was a positive response to the question in the Longitudinal Follow-up
Survey: " . . . ever been told by a doctor, nurse, or other health care provider
that [child's name] has asthma?"
Analyses were performed on SUDAAN software to account for the complex
sampling design,28 and  2 tests
were used for determining differences in proportions.29
Variables were tested individually for an association with history of asthma
in the entire population and African American and white subpopulations separately.
Factors that approached statistical significance (P<.1)
were entered into a forced logistic regression model to investigate independent
associations.
Prevalence and attributable risk calculations were performed on the
basis of nationally weighted sample sizes. Attributable risk estimates included
an estimate of the percentage reduction in a given outcome that would occur
if the risk factor were eliminated from the general population (population
attributable risk percentage) and an estimate of the proportion of an outcome
that is explained by exposure to the risk factor alone (attributable risk
percentage). These calculations were based on the following
formulas30, 31:
PAR% = {P(E)(RR - 1)/[1 + P(E)(RR - 1)]} x 100,
where PAR% indicates population
attributable risk percentage, P(E) indicates proportion of whole population
exposed to risk factor, and RR indicates relative risk of disease; and
AR% = [(ARexposed - ARnonexposed)/ARexposed] x 100,
where AR% indicates attributable risk percentage and AR indicates absolute risk of disease.
RESULTS
In this nationally representative, longitudinal sample of 3-year-olds,
the prevalence of asthma was 7.1%. Asthma prevalence was 21.9% among VLBW
children and 10.9% among MLBW children, compared with 6.7% among children
with normal birth weight (P<.001).
The association between asthma and a number of sociodemographic characteristics
was investigated. In the general population, birth weight, history of maternal
smoking, race, sex, maternal education, maternal age at time of child's birth,
poverty status, and history of other CLD all approached statistical significance;
interval since last live birth, prenatal care, and maternal weight gain during
pregnancy did not. Since many of these variables are interrelated, they were
included in a logistic regression analysis to estimate the independent contribution
of each factor to asthma (Table 1).
After other variables were accounted for, children with VLBW had nearly 3
times the risk of physician-diagnosed asthma compared with those born weighing
2500 g or more. Children in the MLBW category had a smaller but still significant
risk. African American race, male sex, and maternal history of smoking were
also independently associated with increased risk of early-childhood asthma
in the overall population.
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Table 1. Reported Asthma Prevalence and Independent Associations for
Asthma Diagnosis in Selected Characteristics: 1988 National Maternal-Infant
Health Survey and 1991 Longitudinal Follow-up Survey*
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In this sample, a positive response to the question of other chronic
respiratory diseases was the strongest independent predictor of asthma of
all the variables entered into this model. Because this variable was not clearly
defined, its effect on the analysis was evaluated by running the regression
with and without it in the model (data not shown). The statistical conclusions
were not altered with history of CLD excluded from the model. The RR for all
variables, except the birth weight categories, remained the same with and
without CLD in the regression analysis. The RR in the LBW categories increased
with CLD excluded (MLBW, 1.39-1.45; VLBW, 2.86-3.41), suggesting a confounding
relationship between birth weight, CLD, and development of asthma. In a separate
analysis in children with VLBW, CLD was not an independent predictor of asthma.
Weighted sample sizes and the most conservative RR were used for attributable
risk calculations. Table 2 presents
the results of these calculations. The majority of the increased risk for
asthma in children with VLBW (68%) was explained by their birth weight alone.
Approximately 4000 excess cases of early-childhood asthma nationally could
be attributed to LBW. The calculations for attributable risk in children whose
mothers smoked were included for comparison.
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Table 2. Asthma Prevalence and Attributable Risk Calculations Based
on Weighted, National Sample Sizes: 1988 National Maternal-Infant Health Survey
and 1991 Longitudinal Follow-up Survey*
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Separate analyses were run on white and African American children. In
both populations, male sex (odds ratio [OR]white, 1.8; 95% confidence
interval [CI], 1.3-2.5; ORAfrican American, 1.5; 95% CI, 1.2-1.9)
and CLD (ORwhite, 3.9; 95% CI, 2.4-6.1; ORAfrican American, 2.8; 95% CI, 2.0-3.9) were independently associated with asthma. Maternal
education, maternal age at delivery, and poverty status were not independent
contributors to asthma prevalence in both white and African American children.
Interestingly, a history of maternal smoking was not independently associated
with increased risk for asthma in African American children (OR, 1.2; 95%
CI, 0.9-1.6); it was significant in the white population (OR, 1.7; 95% CI,
1.3-2.4). Odds ratios for both VLBW and MLBW were slightly higher for white
children (OR, 3.1; 95% CI, 2.2-4.3; and OR, 1.7; 95% CI, 1.2-2.3, respectively)
compared with African American children (OR, 2.5; 95% CI, 2.0-3.3; and OR,
1.1; 95% CI, 0.8-1.4, respectively). The contribution of VLBW to asthma was
greater in the African American population, however, because of the increased
prevalence of VLBW (population attributable risk percentage, 2.7%).
COMMENT
This study identified a strong independent association between LBW and
asthma in young children that was not equal across LBW categories. These data
are also the first we are aware of to suggest that the impact of LBW on asthma
prevalence is not uniform across ethnic groups. The increased contribution
of LBW to asthma in African American populations was due to the increased
prevalence of LBW in this group alone, not to an increased association between
birth weight and asthma. Recognizing the elevated risk for asthma in an individual
child with LBW may prove useful for explicating the pathophysiology of this
disease, educating providers and parents, and focusing early intervention
programs aimed at reducing asthma burden in the population as a whole and
in specific ethnic communities.
The effect of birth weight on an individual child's risk for developing
asthma was substantial and most pronounced in the lowest birth weight category.
Children with VLBW had nearly twice the risk of being diagnosed as having
asthma compared with MLBW children and nearly 3 times that of children with
normal birth weight. Although the causative factor for asthma development
in the VLBW child has not been clearly identified, children born weighing
less than 1500 g have patterns of reduced pulmonary function similar to those
described in children at risk for transient or early-childhood wheezing.23, 31, 32, 33, 34, 35, 36, 37, 38
It may also be hypothesized that VLBW is a marker for a family or environment
vulnerable to the development of asthma. Further research needs to be done
to assess the potential contribution of each of these factors on asthma development
in the VLBW child.
Enhancing national efforts to reduce LBW and targeting VLBW children,
in particular, for programs to reduce asthma morbidity may result in reduction
of early-childhood asthma burden within a given community. In the individual
child with VLBW, more than half of the increased risk for asthma was explained
by birth weight alone (attributable risk percentage, 68%). Methods aimed at
reducing VLBW in a general population, therefore, should also have an effect
on lowering asthma prevalence. Because of the low prevalence of VLBW in the
average community, however, the change in the overall number of affected children
with asthma can be expected to be modest. A more substantial impact on asthma
prevalence would be seen within African American communities, where LBW is
proportionately more common.
Reducing the incidence of VLBW also may have a noticeable effect on
asthma-related utilization of medical resources. A recent assessment of asthma-related
costs in a Medicaid population showed that mean per capita asthma costs were
approximately 4 times higher in VLBW children than in children with normal
birth weight.39 The gains achieved by targeting
VLBW, therefore, may have the greatest impact on distribution of medical resources
and overall dollars spent in caring for young children with asthma. Again,
these gains may be most significant in African American communities.
There were few differences in independent contributors to asthma development
between African American and white children. The odds for developing asthma
in children with VLBW were smaller in the African American than in the white
population. Confidence intervals overlapped substantially between the 2 groups,
however, making it difficult to infer true difference between the groups.
In addition, it is interesting that maternal smoking was not a significant
independent contributor to asthma prevalence in young African American children.
These data are preliminary and require further research to substantiate their
veracity. If true, however, they may indirectly support the hypothesis initiated
in the literature on bronchopulmonary dysplasia14, 15, 16
that pulmonary function and/or response to prenatal insults or perinatal respiratory
interventions are somehow different in African American children than in white
children.
A large national sample provides many advantages for studying the impact
of a relatively rare event like LBW, including increased power and generalizability
of results. There are limitations, however, to these data specifically. First,
our ability to accurately classify children with a history of bronchopulmonary
dysplasia was limited. Our purpose was to identify the contribution of LBW
to asthma prevalence, regardless of any comorbid conditions that may exist.
In early childhood, however, significant respiratory disease related to prematurity
may obscure the diagnosis of asthma. In several small studies, an increased
risk for asthma symptoms and/or diagnosis has been found in VLBW children,
irrespective of history of bronchopulmonary dysplasia.4, 21, 34, 35, 40
This is also suggested in our data by the lack of independent association
between CLD and asthma in the VLBW group. A history of bronchopulmonary dysplasia,
therefore, may modify the strength of the independent association between
VLBW and asthma, but all VLBW children share this increased risk for asthma.
A second limitation is the potential for selection bias. Identifying
asthmatic children on the basis of parental report alone leaves room for error.
Parental report of physician-diagnosed asthma in a questionnaire format, however,
has been shown to have a high specificity and positive predictive value (95%
and 54%, respectively) compared with exercise challenge41
and physician assessment (85% and 61%, respectively).42
Young children with asthma may be misclassified as normal when their symptoms
are mild and less persistent. The likelihood is greater, therefore, that these
prevalence values are underestimates of true disease burden.
Since no gold standard for defining asthma exists, systematic selection
bias may occur if diagnostic practices are influenced by birth weight. In
LBW infants without comorbid respiratory conditions, physicians may be more
or less likely to attribute wheezing in a LBW child to "asthma" depending
on their belief that wheezing is expected in children born prematurely. Large
national samples should provide an averaging effect by including physicians
who err in both directions. Without a record of quality and quantity of symptoms,
however, the direction and magnitude of any bias effect cannot be accurately
assessed. We would argue, however, that the labeling and treatment of a disease
process as asthma results in a measurable and valid impact on medical resource
utilization even if the diagnosis itself is inaccurate. Investigations into
the pathophysiologic processes of recurrent wheezing in LBW children compared
with children with normal birth weight are needed to clarify whether the disease
processes are the same. A better understanding of physician decision-making
processes also is needed to identify sources of bias in early-childhood asthma
diagnosis.
These data contribute to the continued exploration of the public health
impact of LBW on early childhood asthma. The modest contribution of LBW to
the overall prevalence of asthma in very young children suggests that other
factors are responsible for the increasing asthma prevalence in this age group.
The strength of the individual association between LBW and asthma shown in
this study, however, supports the need for focused intervention in this group
of children. The disproportionate effect of VLBW in racial subpopulations
also warrants targeted intervention programs specifically aimed at reducing
the prevalence of this risk factor. Educational programs, therapeutic trials,
and etiologic research specific for children with LBW may result in substantial
reduction of morbidity in LBW children and improve outcomes in high-risk populations.
AUTHOR INFORMATION
Accepted for publication November 21, 2000.
Presented in part at the 1998 Ambulatory Pediatric Association Annual
Meeting, New Orleans, La, May 3, 1998.
Reprints not available from the authors.
From the Division of Pediatric Pulmonology, Nemours Children's Clinic–Orlando,
Orlando, Fla (Dr Brooks); Department of Pediatrics, General Pediatrics Section,
University of California, Davis, Sacramento (Dr Byrd); American Academy of
Pediatrics, Center for Child Health Research, Rochester, NY (Dr Weitzman);
Department of Pediatrics, University of Rochester School of Medicine and Dentistry,
Rochester (Dr Weitzman and Ms Auinger); and Department of Pediatrics, Children's
Hospital Medical Center of Akron, Northeast Ohio Universities College of Medicine,
Akron, Ohio (Dr McBride).
REFERENCES
| |
1. Mannino DM, Homa DM, Pertowski CA, et al. Surveillance for asthma—United States, 1960-1995. Mor Mortal Wkly Rep CDC Surveill Summ. 1998;47:1-28.
2. Smith DH, Malone DC, Lawson KA, et al. A national estimate of the economic costs of asthma. Am J Respir Crit Care Med. 1997;156:787-793.
FREE FULL TEXT
3. Von Mutius E, Nicolai T, Martinez FD. Prematurity as a risk factor for asthma in preadolescent children. J Pediatr. 1993;123:223-229.
FULL TEXT
|
ISI
| PUBMED
4. Pelkonen AS, Hakulinen AL, Turpeinen M. Bronchial lability and responsiveness in school children born very
preterm. Am J Respir Crit Care Med. 1997;156:1178-1184.
FREE FULL TEXT
5. Seidman DS, Laor A, Gale R, Stevenson DK, Danon YL. Is low birth weight a risk factor for asthma during adolescence? Arch Dis Child. 1991;66:584-587.
FREE FULL TEXT
6. Kelly YK, Brabin BJ, Milligan P, et al. Maternal asthma, premature birth and the risk of respiratory morbidity
in school children in Merseyside. Thorax. 1995;50:525-530.
FREE FULL TEXT
7. Weitzman M, Gortmaker SL, Sobol AM, Perrin JM. Recent trends in the prevalence and severity of childhood asthma. JAMA. 1992;268:2673-2675.
FREE FULL TEXT
8. Mallory GB, Chaney H, Mutich RL, Motoyama EK. Longitudinal changes in lung function during the first three years
of premature infants with moderate to severe bronchopulmonary dysplasia. Pediatr Pulmonol. 1991;11:8-14.
ISI
| PUBMED
9. Kitchen WH, Olinsky A, Doyle LW, et al. Respiratory health and lung function in 8-year-old children of very
low birth weight: a cohort study. Pediatrics. 1992;89:1151-1158.
FREE FULL TEXT
10. Gerhardt T, Hehre D, Feller R, et al. Serial determination of pulmonary function in infants with chronic
lung disease. J Pediatr. 1987;110:448-456.
FULL TEXT
|
ISI
| PUBMED
11. Guyer B, Hoyert DL, Martin JA, et al. Annual summary of vital statistics—1998. Pediatrics. 1999;104:1229-1246.
FREE FULL TEXT
12. Richardson DK, Gray JE, Gortmaker SL, et al. Declining severity adjusted mortality: evidence of improving neonatal
intensive care. Pediatrics. 1998;102:893-899.
FREE FULL TEXT
13. Schwartz J, Gold D, Dockery DW, Weiss ST, Speizer FE. Predictors of asthma and persistent wheeze in a national sample of
children in the US. Am Rev Respir Dis. 1990;142:555-562.
ISI
| PUBMED
14. Palta M, Gabbert D, Weinstein MR, Peters ME. Multivariate assessment of traditional risk factors for chronic lung
disease in very low birth weight neonates. J Pediatr. 1991;119:285-292.
FULL TEXT
|
ISI
| PUBMED
15. Hobar J, McAuliffe T, Adler S, et al. Variability in 28-day outcomes for VLBW infants: an analysis of 11
NICUs. Pediatrics. 1988;82:554-559.
FREE FULL TEXT
16. Avery ME, Tooley W, Keller J, et al. Is chronic lung disease in LBW infants preventable? a survey of 8 centers. Pediatrics. 1987;79:26-30.
FREE FULL TEXT
17. Anderson HR, Bland JM, Peckham CS. Risk factors for asthma up to 16 years of age. Chest. 1987;91(suppl):127S-130S.
18. Schaubel D, Math B, Johansen H, et al. Neonatal characteristics as risk factors for preschool asthma. J Asthma. 1996;33:255-264.
ISI
| PUBMED
19. Sears MR, Holdaway MD, Flannery EM, Herbison GP, Silva P. Parental and neonatal risk factors for atopy, airway hyper-responsiveness
and asthma. Arch Dis Child. 1996;75:392-398.
FREE FULL TEXT
20. Weitzman M, Gortmaker S, Walker DK, Sobol A. Maternal smoking and childhood asthma. Pediatrics. 1990;85:505-511.
FREE FULL TEXT
21. Frischer T, Kuehr J, Meinert R, Karmaus W, Urbanek R. Risk factors for childhood asthma and recurrent wheezy bronchitis. Eur J Pediatr. 1993;152:771-775.
FULL TEXT
|
ISI
| PUBMED
22. Weitzman M, Gortmaker S, Sobol A. Racial, social and environmental risks for childhood asthma. AJDC. 1990;144:1189-1194.
23. Martinez FD, Wright AL, Taussig LM, et al. Asthma and wheezing in the first six years of life. N Engl J Med. 1995;332:133-138.
FREE FULL TEXT
24. Persky VW, Slezak J, Contreras A, et al. Relationships of race and socioeconomic status with prevalence, severity
and symptoms of asthma in Chicago school children. Ann Allergy Asthma Immunol. 1998;81:266-271.
ISI
| PUBMED
25. Ernst P, Demissie K, Joseph L, et al. Socioeconomic status and indicators of asthma in children. Am J Respir Crit Care Med. 1995;152:570-575.
ABSTRACT
26. Lewis S, Richards D, Bynner J, Butler N, Britton J. Prospective study of risk factors for early and persistent wheezing
in childhood. Eur Respir J. 1995;8:349-356.
ABSTRACT
27. Oliveti JF, Kercsmar CM, Redlin S. Pre- and perinatal risk factors for asthma in inner city African-American
children. Am J Epidemiol. 1996;143:570-577.
FREE FULL TEXT
28. Shah BV, Barnwell BG, Hunt PN, LaVange LM. SUDAAN User's Manual, Release 6.20. Research Triangle Park, NC: Research Triangle Institute; 1992.
29. Fleiss JL. Statistical Methods for Rates and Proportions. 2nd ed. New York, NY: John Wiley & Sons; 1981.
30. Lilienfeld DE, Stolley PD. Foundations of Epidemiology. New York, NY: Oxford University Press; 1994:202-204.
31. Gordis L. More on risk: estimating the potential for prevention. In: Epidemiology. Philadelphia, Pa: WB Saunders
Co; 1996:156-161.
32. Chan KN, Noble-Jamieson CM, Elliman A, et al. Lung function in children of low birth weight. Arch Dis Child. 1989;64:1284-1293.
FREE FULL TEXT
33. Yuksel B, Greenough A. Relationship of symptoms to lung function abnormalities in preterm
infants at follow-up. Pediatr Pulmonol. 1991;11:202-206.
ISI
| PUBMED
34. Galdes-Sebaldt M, Sheller JR, Grogaard J, et al. Prematurity is associated with abnormal airway function in childhood. Pediatr Pulmonol. 1989;7:259-264.
ISI
| PUBMED
35. Mansell AL, Driscoll JM, James LS. Pulmonary follow-up of moderately low birth weight infants with and
without respiratory distress syndrome. J Pediatr. 1987;110:111-115.
FULL TEXT
|
ISI
| PUBMED
36. Clarke JR, Reese A, Silverman M. Bronchial responsiveness and lung function in infants with lower respiratory
tract illness over the first six months of life. Arch Dis Child. 1992;67:1454-1458.
FREE FULL TEXT
37. Voter KZ, Henry MM, Stewart PW, et al. Lower respiratory illness in early childhood and lung function and
bronchial reactivity in adolescent males. Am Rev Respir Dis. 1988;137:302-307.
ISI
| PUBMED
38. Stick SM, Arnott J, Turner DJ, et al. Bronchial responsiveness and lung function in recurrent wheezy infants. Am Rev Respir Dis. 1991;144:1012-1015.
ISI
| PUBMED
39. Brooks AM, McBride JT, Barth R, McConnochie K, Swantz R, Szilagyi P. Contribution of prematurity to asthma burden in the first three years
of life [abstract]. Pediatr Res. 1999;45:585A.
40. Greenough A, Giffin FJ, Yuksel B, Dimitriou G. Respiratory morbidity in young school children born prematurely: chronic
lung disease is not a risk factor? Eur J Pediatr. 1996;155:823-826.
ISI
| PUBMED
41. Demissie K, White N, Joseph L, Ernst P. Bayesian estimation of asthma prevalence and comparison of exercise
and questionnaire diagnostics in the absence of a gold standard. Ann Epidemiol. 1998;8:201-208.
FULL TEXT
|
ISI
| PUBMED
42. Jenkins MA, Clarke JR, Carlin JB, et al. Validation of questionnaire and bronchial hyperresponsiveness against
repiratory physician assessment in the diagnosis of asthma. Int J Epidemiol. 1996;25:609-616.
FREE FULL TEXT
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Thorax 2007;62:231-236.
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Comparing Individual- and Area-based Socioeconomic Measures for the Surveillance of Health Disparities: A Multilevel Analysis of Massachusetts Births, 1989-1991
Subramanian et al.
Am J Epidemiol 2006;164:823-834.
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Low Birthweight and Asthma Among Young Urban Children
Nepomnyaschy and Reichman
AJPH 2006;96:1604-1610.
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Are Children of Moderately Low Birth Weight at Increased Risk for Poor Health? A New Look at an Old Question
Stein et al.
Pediatrics 2006;118:217-223.
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Heterogeneity of Childhood Asthma Among Hispanic Children: Puerto Rican Children Bear a Disproportionate Burden
Lara et al.
Pediatrics 2006;117:43-53.
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Impact of Low Birth Weight on Early Childhood Asthma in the United States
Macginnitie and Schneider
Pediatrics 2002;110:444-444.
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Complex interactions in complex traits: obesity and asthma
Tantisira and Weiss
Thorax 2001;56:ii64-74.
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