Polio Extraimmunization in Children Younger Than 2 Years After Changes in
Immunization Recommendations
Loren K. Mell, Robert L. Davis, John P. Mullooly, Steven B. Black, Henry R.
Shinefield, Kenneth M. Zangwill, Joel I. Ward, S. Michael Marcy and Robert T. Chen
Pediatrics 2003;111;296-301
DOI: 10.1542/peds.111.2.296
The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://www.pediatrics.org/cgi/content/full/111/2/296
PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly
publication, it has been published continuously since 1948. PEDIATRICS is owned, published,
and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk
Grove Village, Illinois, 60007. Copyright © 2003 by the American Academy of Pediatrics. All
rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.
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Polio Extraimmunization in Children Younger Than 2 Years After
Changes in Immunization Recommendations
Loren K. Mell, BS*‡; Robert L. Davis, MD, MPH*§; John P. Mullooly, PhD储; Steven B. Black, MD¶;
Henry R. Shinefield, MD¶; Kenneth M. Zangwill, MD#; Joel I. Ward, MD#; S. Michael Marcy, MD**; and
Robert T. Chen, MD‡‡, for the CDC Vaccine Safety Datalink Project
ABSTRACT. Objective. To investigate trends over
time in polio extraimmunization among children in 4
large health maintenance organizations and to study the
association with recent changes in polio immunization
policy.
Methods. Using 176 169 children who were born after
1994 and enrolled for their first 2 years of life, we assessed rates and trends of polio extraimmunization in the
Vaccine Safety Datalink project. We used logistic regression to test the association of extraimmunization with
different polio immunization schedules and with sociodemographic characteristics and used Poisson regression
to test changes in rates over time.
Results. Overall, 10.5% were extraimmunized for poliovirus; children on the all inactivated polio virus or
sequential schedule were one half as likely as those on
the all oral polio virus schedule to be extraimmunized by
2 years of age. There was a significant decrease in extraimmunization over time, with <5% of children born at the
end of 1997 being extraimmunized, compared with >15%
at the beginning of 1994.
Conclusions. Poliovirus extraimmunization rates have
fallen dramatically in association with the changeover to the all inactivated polio virus schedule. Pediatrics
2003;111:296 –301; extraimmunization, polio vaccine.
ABBREVIATIONS. OPV, oral polio virus; IPV, inactivated polio
virus; DTP, diphtheria and tetanus toxoids and whole-cell pertussis; DTaP, diphtheria and tetanus toxoids and acellular pertussis;
Hib, Haemophilus influenzae type b; HBV, hepatitis B virus; MMR,
measles-mumps-rubella; HMO, health maintenance organization;
GHC, Group Health Cooperative of Puget Sound; SCK, Southern
California Kaiser Permanente Health Care Program; NCK, Northern California Kaiser Permanente Health Care Program; NWK,
Kaiser Permanente Northwest.
From the *Center for Health Studies, Group Health Cooperative, Seattle,
Washington; ‡University of Chicago, Pritzker School of Medicine, Chicago,
Illinois; §University of Washington, Departments of Pediatrics and Epidemiology, Seattle, Washington; 储Center for Health Research, Northwest Kaiser Permanente, Portland, Oregon; ¶Division of Research, Kaiser Permanente of Northern California, Oakland, California; #UCLA Center for
Vaccine Research, Harbor-UCLA Medical Center, Torrance, California;
**Kaiser-UCLA Vaccine Research Group, Southern California Kaiser, Permanente, Panorama City, California; and ‡‡National Immunization Program, Vaccine Safety and Development Activity, Centers for Disease Control and Prevention, Atlanta, Georgia.
Dr Mell performed this work while with Center for Health Studies, Group
Health Cooperative.
Received for publication Jun 3, 2002; accepted Sep 23, 2002.
Reprint requests to (R.L.D.) University of Washington Department of Pediatrics, Box 358853, 146 North Canal St, Ste 300, Seattle, WA 98103. E-mail:
rdavis@u.washington.edu
PEDIATRICS (ISSN 0031 4005). Copyright © 2003 by the American Academy of Pediatrics.
296
C
hildhood immunizations provide an effective
means of reducing morbidity and mortality
from infectious disease. Efforts to ensure
timely and thorough administration of immunizations have significantly increased immunization coverage rates among US children. As a result of these
efforts, current coverage rates have reached an alltime high, with a corresponding decline in the incidence of vaccine-preventable diseases.1,2
Although thorough immunization coverage remains a top priority of US vaccination policy, recent
attention has turned to understanding better and
ameliorating the problem of extraimmunization. Extraimmunization wastes resources, causes unnecessary pain, and increases children’s risk for adverse
events after vaccination. Extraimmunization may result from either superfluous vaccination (vaccination
after successful completion of a series) or early vaccination, which often necessitates correction with additional vaccination to ensure adequate immune response or to meet school requirements. Early
vaccinations are those given before a minimum age
has been achieved or a minimum between-dose time
interval has elapsed.
A recent study of children aged 19 to 35 months
showed that extraimmunization is a frequent and
costly problem.3 This study found that 21% of children who were born between February 1994 and
May 1996 were extraimmunized for 1 or more of the
following antigens: poliovirus (oral [OPV] or inactivated [IPV]), diphtheria and tetanus toxoids and
whole-cell or acellular pertussis (DTP or DTaP), Haemophilus influenzae type b (Hib), hepatitis B virus
(HBV), or measles-mumps-rubella (MMR). Poliovirus was the antigen most commonly given in excess,
with 14.1% of children extraimmunized for this series. For each of the other vaccines, fewer than 5% of
children were extraimmunized. Another, smaller
study estimated that 18% of children were extraimmunized for their age, and 9% were extraimmunized
for polio.4
These estimates of polio extraimmunization rates,
although valuable, were based on data that preceded
or coincided with major changes in polio immunization recommendations that occurred between 1997
and 20005–9 (Table 1). Recent data indicate that extraimmunization rates have begun to decline since
these policy changes were put in effect, with 10.6% of
children in a 2000 survey extraimmunized, com-
PEDIATRICS Vol. 111 No. 2 February 2003
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Childhood Polio Immunization Recommendations by Age 2: 1994 to 2000
TABLE 1.
Year
ACIP
AAP
1994–1996
1997
OPV at 2, 4, and 6 mo
IPV at 2 and 4 mo; OPV at 12–18 mo
1998
IPV at 2 and 4 mo; OPV at 12–18 mo
1999
IPV at 2 and 4 mo; OPV at 12–18 mo
2000
IPV at 2, 4, and 6–18 mo
OPV at 2, 4, and 6–18 mo
IPV at 2 and 4 mo; OPV at 12–18 mo OR
IPV at 2, 4, and 12–18 mo OR
OPV at 2, 4, and 6–18 mo
IPV at 2 and 4 mo; OPV at 6–18 mo OR
IPV at 2, 4, and 6–18 mo OR
OPV at 2, 4, and 6–18 mo
IPV at 2 and 4 mo; OPV at 6–18 mo OR
IPV at 2, 4, and 6–18 mo
IPV at 2, 4, and 6–18 mo
ACIP indicates Advisory Committee on Immunization Practices; AAP, American Academy of Pediatrics.
pared with 21.1% of children surveyed in 1997.10
Because estimates of polio extraimmunization rates
that reflect current vaccination practices are lacking,
we evaluated the impact of changing recommendations on polio extraimmunization in children
younger than 2 years.
METHODS
Study Population and Immunization Data
This study used data from the Vaccine Safety Datalink project
supported by the National Immunization Program at the Centers
for Disease Control and Prevention. The data include demographic information and vaccination histories of children enrolled
at 4 health maintenance organizations (HMOs): the Group Health
Cooperative of Puget Sound (GHC; Seattle, WA), Kaiser Permanente Northwest (NWK; Portland, OR), Kaiser Permanente Medical Program of Northern California (NCK; Oakland, CA), and
Southern California Kaiser Permanente Health Care Program
(SCK; Los Angeles, CA).
Vaccine Safety Datalink data have been used in a variety of
childhood immunization studies.11 Each child possesses a unique
identifier, and demographic data include birth date, gender, Medicaid status, and, with the exception of GHC, race. Vaccination
histories were derived from computerized immunization tracking
systems maintained by each HMO and included data concerning
vaccination date, type of vaccine administered, and clinic at which
the vaccine was administered.
Our study analyzed 176 169 children who were born between
January 1, 1994, and December 31, 1997 (for NCK, SCK, and
NWK), or December 31, 1996 (for GHC), and were continuously
enrolled for the first 2 years of life. The different endpoints for the
time periods were used because of differences in data availability
at the time of our analysis. The enrollment requirement was made
to ensure completeness of immunization histories. The time period corresponds to the cohort of children who reached 2 years of
age between January 1, 1996, and December 31, 1999. Using the
same time period in the calculation of extraimmunization rates
over time, we studied all children who were aged 1 to 2 and
enrolled between January 1, 1996, and December 31, 1999 (for
NCK, SCK, and NWK), or December 31, 1998 (for GHC), and
continuously enrolled from birth (N ⫽ 253 427).
Immunization Definitions
Because no more than 3 polio immunizations before 2 years of
age were recommended during the study period, we considered
children who received 4 or more polio immunizations before 2
years of age to be extraimmunized for polio. Children with at least
3 polio immunizations were categorized according to the type of
vaccine administered for their first 3 immunizations: all-OPV,
all-IPV, IPV-IPV-OPV sequential schedule, or a nonstandard mix
of IPV and OPV.
To compare rates of polio extraimmunization to previous studies, we calculated the percentage of children in our sample who
were extraimmunized by 2 years of age. However, this type of
analysis did not allow us to determine when the extraimmunizations occurred. Therefore, we also assessed the rate of extraimmunization occurrences among 1- to 2-year-olds as a function of time,
to compare these rates before and after the introduction of recom-
mendation changes. To evaluate extraimmunization over time, for
each month, we divided the number of children who were between age 1 and 2 years and were extraimmunized by the total
number of children who were between 1 and 2 years at some time
in that month. Children were required to be enrolled continuously
from birth through the end of the given month. The 1- to 2-yearold age range was chosen because no children in our sample who
were younger than 1 year were extraimmunized.
To evaluate whether any trends seen among polio immunizations were also seen in other vaccine series, we calculated extraimmunization rates for DTP/DTaP. Children who received 5 or
more DTaP vaccinations before the age of 2 years were considered
TABLE 2.
Descriptive Statistics
Number
Total
Site
GHC
NCK
SCK
NWK
Birth year
1994
1995
1996
1997
Gender
Male
Female
Race
White
Black
Other
Unknown
Medicaid
Never on Medicaid
Ever on Medicaid
Unknown
Clinic continuity
All vaccinations at same clinic
Vaccinations at different clinics
Vaccination sites unknown
Immunization status
Never immunized
Underimmunized
Properly immunized
All-OPV
All-IPV
IPV-IPV-OPV
Other
Extraimmunized
First 3 vaccines OPV-OPVOPV
First 3 vaccines IPV-IPV-IPV
First 3 vaccines IPV-IPV-OPV
Other
176 169
Percentage
100
7329
76 994
82 562
9284
4.2
43.7
46.9
5.3
42 342
43 612
46 384
43 831
24.0
24.5
26.3
24.9
90 204
85 963
51.2
48.8
86 546
12 710
40 778
36 135
49.1
7.2
23.2
20.5
169 653
5516
1000
96.3
3.1
0.6
122 735
7540
45 984
69.7
4.3
26.1
9121
13 860
5.2
7.9
113 813
2754
16 235
1861
64.6
1.6
9.2
1.1
16 888
9.6
161
861
615
0.1
0.5
0.3
Sample: All children born January 1, 1994, through December 31,
1997, continuously enrolled from birth through 2 years of age.
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TABLE 3.
Regression Analysis Results
Characteristic
% Extraimmunized
OR (95% CI)
All-OPV schedule
All-IPV schedule
IPV-IPV-OPV schedule
Other mix of IPV and OPV
Third vaccination before 7 mo
Born in 1994
Born in 1995
Born in 1996
Born in 1997
Male
Female
Non-Medicaid
Medicaid
Medicaid status unknown
White
Black
Other
Race unknown
All immunizations at same clinic
Immunizations at different clinics
Clinic data unknown
12.9*
5.5*
5.0*
24.4*
15.1*
14.3
11.1
9.5
7.4
10.6
10.5
10.6
8.2
2.9
10.5
9.6
12.1
9.1
10.2
21.4
9.5
Referent*
0.67 (0.57–0.79)*
0.72 (0.66–0.78)*
3.02 (2.73–3.33)*
2.32 (2.23–2.41)*
Referent
0.67 (0.64–0.70)
0.53 (0.51–0.56)
0.50 (0.48–0.53)
Referent
1.00 (0.97–1.03)
Referent
1.03 (0.93–1.14)
0.71 (0.48–1.04)
Referent
0.96 (0.90–1.03)
1.20 (1.16–1.25)
1.01 (0.97–1.06)
Referent
2.87 (2.70–3.05)
1.02 (0.98–1.07)
OR indicates odds ratio; CI, confidence interval.
* Among children with at least 3 polio vaccinations.
to be extraimmunized for diphtheria, tetanus, and pertussis. To
have greater confidence that each automated record represented a
distinct vaccination, we considered vaccinations of the same type
given within 1 week of each other to be duplicate record entries.
These duplicate records (0.2% of polio and 0.5% of DTP/DTaP
immunizations) were eliminated from our analyses.
Children who received fewer than 3 polio immunizations before 2 years of age were considered to be underimmunized. Children who received 3 immunizations but had 1 or more immuni-
zations given prematurely, without receiving a make-up dose,
were also considered to be underimmunized. Minimum age for
vaccination and minimum between-dose intervals were determined according to the prevailing recommendations at the time
each vaccination was administered.
Finally, a number of advisory committees have suggested that
the administration of extra antigens is acceptable when a combination vaccine would reduce the required number of injections (or
if it is the only means of delivering the indicated antigen).12
Fig 1. Percentage of children extraimmunized by age 2, 1994 to 1997.
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POLIO EXTRAIMMUNIZATION AND VACCINE SCHEDULE CHANGES
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Therefore, when evaluating combination vaccines (eg, DTP-HIB),
an extraimmunization was counted as such only when the extraimmunization was present for both antigens.
Statistical Analysis
Statistical analyses were performed using SAS Software (SAS
Inc, Cary, NC) and Stata Statistical Software (Stata Corp, College
Station, TX). We used logistic regression to test whether polio
schedule type (all-OPV, all-IPV, IPV-IPV-OPV sequential schedule, or other mix of IPV and OPV) was associated with the probability of a child’s being extraimmunized by 2 years of age. Because we hypothesized that children who were up-to-date at an
earlier age were at greater risk to be extraimmunized, our model
adjusted for the number of polio immunizations received before 7
months of age. Sociodemographic factors of interest included birth
cohort, gender, Medicaid status, race (white, black, or other), and
continuity of care. Models of immunization error rates over time
were performed using Poisson estimation. The regression model
tested for the significance of a time trend variable.
RESULTS
Most children were enrolled at either NCK (43.7%)
or SCK (46.9%; Table 2). Among children with available data, 61.8% were white and 9.1% were black,
3.2% were on Medicaid, and 94.2% received all of
their vaccinations at the same clinic. Overall, 5.2% of
children were never immunized, 7.9% of children
were underimmunized, 76.5% were properly immunized, and 10.5% were extraimmunized for poliovirus. Of children who were properly immunized,
84.5% received the all-OPV schedule, 2.0% received
the all-IPV schedule, 12.1% received the IPV-IPVOPV sequential schedule, and 1.4% received a nonstandard mix of IPV and OPV. Of children who were
extraimmunized, 91.2% received the all-OPV schedule, 0.9% received the all-IPV schedule, 4.6% re-
ceived the IPV-IPV-OPV sequential schedule, and
3.3% received a nonstandard mix of IPV and OPV.
The results from the regression analysis (Table 3)
indicate a significant downward trend in extraimmunization rates over time. Children on the all-IPV or
IPV-IPV-OPV sequential schedule were approximately two thirds to three fourths as likely as children on the all-OPV schedule to be extraimmunized
by 2 years of age. Children who received a nonstandard mix of IPV and OPV were 3 times as likely to be
extraimmunized. Children who received a third polio vaccination before age 7 months were 2.3 times as
likely to be extraimmunized for polio. Whites and
blacks were less likely to be extraimmunized than
children of other races. Continuity of care played a
significant role; children who received 1 or more
vaccinations at different clinics were 2.6 times as
likely to be extraimmunized.
Figure 1 shows the downward trend across birth
cohorts in the percentage of children extraimmunized. More than 15% of children who were born at
the beginning of 1994 were extraimmunized, compared with fewer than 5% of children who were born
at the end of 1997. The downward trend was fairly
consistent with the exception of the first half of 1997,
when the rates increased before declining again. In
contrast, the percentage of children who were extraimmunized for DTP/DTaP was relatively constant
(between 1% and 2%), with a slight increase occurring in 1997.
Figure 2 shows a similar trend in the number of
extraimmunizations per enrollee between the ages of
Fig 2. Polio extraimmunization among 1- to 2-year-olds, 1996 to 1999, all sites.
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299
1 and 2 years. Between 1996 and 1999, this rate fell
from ⬎1% of enrollees extraimmunized in a given
month to ⬍0.2%. The rate trends downward in 1996,
plateaus in 1997 and early 1998, then declines precipitously until the end of 1999. Poisson analysis
confirmed that the decrease in extraimmunization
over time was statistically significant (P ⬍ .001) and
that this trend was significantly greater after 1998
than before 1998 (P ⬍ .001).
There was a rapid decline in all-OPV use after the
recommendation changes (Fig 3). Use of OPV began
to decline among children who were born in the
latter half of 1996. By mid-1997, children were more
likely to be placed on an alternative schedule. Of
note is that the decline in extraimmunization preceded the decline in OPV use, suggesting that not all
of the decrease in extraimmunization was attributable to IPV use.
When we analyzed the data by site, we found
some differences. All sites showed a generalized
downward trend in both percentage of children extraimmunized and the number of extraimmunizations per enrollee. One site had a higher percentage
of children extraimmunized (13.7%) than the other 3
(9.9%, 9.0%, and 7.7%). Also, the transient increase in
extraimmunization among children who were born
in the first half of 1997 was observed at 2 of the 3
sites; 1 site did not include data for children who
were born in 1997.
DISCUSSION
A strength of this study was the ability to assess
changes in extraimmunization in time periods before
and after the new recommendations, using population-based data from 4 large HMOs. Fewer than 5%
of children who were born in the last quarter of 1997
were extraimmunized, compared with 11.1% of children in the preceding 15 quarters. These results support previous estimates of poliovirus extraimmunization rates before major changes in vaccination
recommendations were instituted. However, our
analysis demonstrates that poliovirus extraimmunization rates have fallen notably in association with
the changeover to the all-IPV schedule. This study
suggests that low rates of poliovirus extraimmunization are achievable with the current all-IPV schedule.
Our analysis also suggests that policy changes
may have led to transient rises in polio extraimmunization rates. Extraimmunization rates had begun to
decline before the introduction of IPV. These rates
leveled off at the time of IPV introduction but resumed the downward trend shortly thereafter. One
possibility is that the changes in polio immunization
policy caused some short-lived confusion, which in
turn increased the erroneous administration of polio
vaccine. However, both the anticipation of and reaction to recommendation changes may have increased
provider awareness concerning correct polio vaccination practice, leading overall to fewer errors. This
Fig 3. Change in type of polio immunization schedule administered, by month, 1994 to 1997.
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POLIO EXTRAIMMUNIZATION AND VACCINE SCHEDULE CHANGES
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might account for the modest decline in extraimmunization preceding IPV introduction and the rapid
decline that followed.
The association of low extraimmunization rates
with the changeover to IPV may also be attributable
in part to a higher threshold for dispensation of
injectable vaccines as a result of the pain associated
with their administration. Rates of DTP/DTaP extraimmunization were relatively constant during the
same time period, suggesting that the decline was
specific to changes in polio vaccination practices
rather than the result of a generalized downward
trend in extraimmunization for all vaccines.
This study had several limitations. Our data were
not comprehensive enough to allow stratification by
certain, potentially relevant patient characteristics,
such as enrollment in Women, Infants and Children,
Head Start, and so forth. Because our sample was
confined to HMO enrollees, our findings may not be
representative of the population of US children. In
addition, the continuous enrollment criterion excluded children who switched health plans during
their first 2 years of life. Such children are probably
predisposed to extraimmunization because they receive their immunizations from different providers,
who may or may not have complete immunization
histories. Therefore, our data probably represent a
low-end estimate of the true national rate of extraimmunization. Finally, it is likely that unmeasured
factors also contributed to the observed decline in
extraimmunization. Although it may be difficult to
perform additional studies of this topic in the private
sector or among patients who switch plans repeatedly, we believe that such studies are needed.
More recent rates of polio extraimmunization are
lower than estimates in the period preceding IPV
introduction and are similar to extraimmunization
rates for other vaccine series. Despite this decline,
polio represents only 1 vaccine in an extensive vaccination regimen. When all vaccinations are considered, a high percentage of children may be extraimmunized for any 1 vaccine. As new vaccines continue
to be added to an already complex vaccination
schedule and as new combinations of vaccines become available, the problem of extraimmunization
will remain. It thus will be important to monitor
rates of extraimmunization in the future, as is currently done for underimmunization. As families
move and change providers in our highly mobile
society, a single solution to ameliorate this problem
is lacking. As a common repository of data, immunization registries hold promise, but their widespread utilization faces many challenges before most
physicians embrace them. The ability of registries to
reduce extraimmunization remains to be shown. Our
results also suggest that use of oral vaccines may be
related to higher rates of extraimmunization. More
attention to this problem in the context of oral vaccination may be warranted.
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Polio Extraimmunization in Children Younger Than 2 Years After Changes in
Immunization Recommendations
Loren K. Mell, Robert L. Davis, John P. Mullooly, Steven B. Black, Henry R.
Shinefield, Kenneth M. Zangwill, Joel I. Ward, S. Michael Marcy and Robert T. Chen
Pediatrics 2003;111;296-301
DOI: 10.1542/peds.111.2.296
Updated Information
& Services
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