PEDIATRICS Vol. 108 No. 1 July 2001, pp. 54-60
Intussusception, Rotavirus Diarrhea, and Rotavirus Vaccine Use Among Children in New York State
,, and
From the * New York State Department of Health, Albany, New
York; Objective. To describe epidemiologic
features of intussusception and rotavirus diarrhea in New York, to
examine the baseline incidence and trends over time, and to ascertain
whether an excess of cases occurred in the 9 months of vaccination with
the newly licensed rotavirus vaccine.
Methods. Hospital discharge data from 1989 through 1998 were reviewed for children (<1 year old) whose primary or secondary
diagnosis was coded as intussusception or rotavirus diarrhea.
Characteristics of patients admitted for intussusception and rotavirus
diarrhea were compared, and trends over time were examined. For a
subset of patients, medical records and vaccine histories for
intussusception hospitalizations from October 1998 through June 1999 were analyzed. The number of intussusception cases attributable to
rotavirus vaccine was calculated based on the penetration of the
vaccine (21%) and a range of excess risks of intussusception among
vaccinated children as estimated by the National Immunization Program
(NIP).
Results. From 1989 through 1998, 1450 intussusception-associated hospitalizations were reported in children
<1 year old (average annual incidence 5.4/10 000). Among these
children, 47% were treated medically and 53% had surgery, with 9%
needing surgical resection. The incidence of intussusception declined
over time from 6.1 per 10 000 in 1989 to 3.9 per 10 000 in 1998. Intussusception hospitalizations occurred throughout the year, whereas
rotavirus-associated hospitalizations peaked from February to April. Of
20 patients with intussusception whose hospitalization charts were
reviewed, 5 had received rotavirus vaccine. All 5 were hospitalized
after their first dose of vaccine, were admitted before 7 months of
age, were white, and had private insurance. A total of 81 cases
of intussusception occurred during the 9-month period of rotavirus
vaccination, compared with 78 during the same period in the
prevaccination year. The number of excess intussusception cases
observed (n = 3) was lower than expected using the
NIP estimate of excess risk (1.8) among rotavirus vaccinated children
(n = 12) but not significantly different from the
risks identified in the NIP cohort studies (1 in 12 000).
Conclusion. Our data suggest that in New York the rate of
intussusception has declined, and approximately 1 child in 2600 develops intussusception before 1 year of age. The different
seasonality between intussusception and rotavirus-related
hospitalizations suggests that if any causal association exists, it
must be small. Unlike other studies, analysis of New York hospitalized
discharge data failed to show an appreciable increase in the incidence
of intussusception after introduction of the rotavirus
vaccine.
Department of Epidemiology, School of Public Health, State
University at Albany, New York; § Epidemic Intelligence Service (State
Branch), Centers for Disease Control and Prevention, Atlanta, Georgia;
and Viral Gastroenteritis Section, Division of Viral and Rickettsial
Diseases, National Center for Infectious Diseases, Centers for Disease
Control and Prevention, Atlanta, Georgia.
ABSTRACT
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Methods
Results
Discussion
References
In August 1998, the United States became the first country
to license a rotavirus vaccine to prevent diarrhea in children. The
vaccine was immediately recommended by the Centers for Disease Control
and Prevention's (CDC's) Advisory Committee on Immunization Practices
and the American Academy of Pediatrics for the routine immunization of
children as an oral vaccine on a 2-, 4-, and 6-month schedule.1,2 Immunization began in the fall of 1998, and
by July 1999 an estimated 1.5 million doses had been administered to
about 800 000 children. In July 1999, reports of intussusception
associated with the vaccine led to a suspension of the program and an
intense investigation by CDC's National Immunization Program (NIP)
into the possible association between the vaccine and
intussusception.3 By October, these investigations had
identified a significant excess number of intussusception cases among
vaccinees that occurred in the first week after receipt of the first
dose.4 Although the CDC investigation had identified a
significant risk of intussusception immediately after vaccination,
estimates of the excess risk attributable to the vaccine varied widely
because the absolute risk was small, different methods were used to
arrive at national figures, and basic issues concerning the
pathogenesis of intussusception remained unanswered. For instance, it
was not clear whether the risk observed was truly excess or whether the
vaccine was triggering intussusception in children who might have an
underlying predisposition for this condition, which would have
otherwise appeared later. Such a triggering effect has been observed
for febrile convulsions immediately after diphtheria-tetanus-pertussis
vaccination, with no excess risk by the end of the year. The initial
relative risk for intussusception was reported as being 1.8 for
recipients of the vaccine,5 and the attributable risk
based on a separate cohort study ranged from 1 case of intussusception
in 4500 to 1 in 12 000 children vaccinated.
New York State, like more than 30 other states, maintains computerized
records of hospital discharges from which descriptive epidemiologic
data on common medical conditions can be derived. For example, when 5 cases of intussusception were reported after rotavirus vaccination
during the prelicensure period, we queried our hospital discharge
database to determine whether the marked winter seasonality of
rotavirus diarrhea also occurred with intussusception.6 The lack of seasonal concordance we observed suggested that
intussusception probably was not associated with natural rotavirus
diarrhea. We also used these data to derive estimates of the background
incidence of intussusception hospitalizations among infants in New York State in calculating the risk attributable to rotavirus vaccine.
When the problem of intussusception associated with the use of
rotavirus vaccine was identified, we estimated that approximately 21%
(~52 000) of infants in the birth cohort of New York State (248 700
in 1998) may have received the rotavirus vaccine based on vaccine
distribution. If the excess risk associated with the vaccine was as
predicted, our hospital discharge data could be used to estimate the
magnitude of the excess number of cases that might be expected as well
as the benefit of the vaccine measured as a decrease in the number of
hospitalizations for childhood diarrhea. Because most of the
intussusception cases occurred in the week after receipt of the first
dose, these data would be most rapidly available, whereas an assessment
of the decrease in hospitalizations for rotavirus diarrhea would entail
waiting for 1 or 2 winter rotavirus seasons. In this study, we sought to describe the epidemiology of intussusception- and
rotavirus-associated hospitalizations in New York, examine the baseline
incidence for intussusception and trends over time, and determine
whether there had been an excess number of cases in the 9 months of the
rotavirus vaccination program that could be attributable to the use of
the newly licensed vaccine.
In New York State, all general acute care hospitals and
hospital-based ambulatory surgical facilities are required to submit inpatient data to the Statewide Planning and Research Cooperative System (SPARCS).7 Hospital discharge data for 1989 through 1998 from SPARCS for children <1 year old who had intussusception (International Classification of Diseases, 9th Revision, Clinical Modification [ICD-9-CM] code 560.0)8 listed as
their primary or any secondary diagnosis were included for analysis.
The procedures performed during hospitalization were examined to
distinguish children whose intussusception was treated medically or
surgically with simple reduction or resection. A surgical resection was
defined as a procedure recorded using the following selected ICD-9-CM codes: partial resection of small intestine
(45.62), multiple segmental resection of large intestine (45.71),
cecectomy (45.72), right hemicolectomy (45.73), and revision of
anastomosis of small intestine (46.93). A surgical reduction was
defined as any of the following procedures that were performed during a
laparotomy (54.11, 54.19) and in which the intestine was manipulated
but not opened: intra-abdominal manipulation of intestine, small
intestine, large intestine (46.80-46.82); biopsy of lymphatic
structure (40.11); open biopsy of small intestine (45.15); suture of
laceration of large intestine (46.75); and appendectomy (47.0-47.1).
This approach did not identify patients who might have been treated
medically as outpatients, and we did not perform chart reviews to
confirm the coded diagnosis.
We examined trends in hospitalizations from intussusception by age,
sex, race, insurance provider, season, length of hospital stay, and
hospital cost. The annual hospital incidence rates per 10 000 children
<1 year old were calculated using the census population estimated by
age, sex, and race for the 10-year period 1989 through 1998. Trends
were tested for significance using the We further examined the descriptive epidemiology of diarrheal
hospitalizations for children <1 year old for the period 1989 through
1998 for which the following ICD-9-CM codes were listed as
the primary or any secondary diagnosis: bacterial diarrhea (001-005,
008.0-008.5, excluding 003.2); parasitic diarrhea (006-007, excluding
006.2-006.6); viral diarrhea (008.6 and 008.8); and diarrhea of
undetermined etiology (009.0-009.3, 558.9).8 Monthly
trends for diarrhea were compared with the same time trends for
intussusception. In 1993, an ICD-9-CM code for rotavirus
diarrhea was introduced (008.61), and these data were also examined for the period 1993 through 1998.
As part of the investigation of the association of rotavirus vaccine
and intussusception conducted by the NIP, all cases of intussusception
were ascertained for hospitals that accounted for 80% of
intussusception cases for children <1 year old in New York State
outside of New York City (where care data were not available to the
authors). Hospital admission notes and discharge summaries were
examined from 20 intussusception cases that occurred between October
1998, when the vaccine was introduced, and June 1999, when vaccination
was stopped, and linked to the child's vaccination history obtained
from the health care providers of these infants. The characteristics of
children who received rotavirus vaccine were compared with those
who did not. Furthermore, the number of intussusception cases was
compared in the 9-month period during rotavirus vaccination (October
1998 to June 1999) and the same 9-month period in the previous year
before the vaccine was licensed. The expected number of excess
intussusception cases was calculated based on the penetration of the
vaccine in New York State and a range of excess risks of
intussusception among vaccinated children estimated by the
NIP.5
For the period 1989 through 1998, 1450 infants were hospitalized
for intussusception in New York State, of whom 47% (685) were treated
medically, 43% needed surgical reduction, and 9% needed surgical
resection. Of these, 3 patients died while hospitalized, for a case
fatality rate of 2.1 per 1000 intussusceptions. The number (and
incidence) of intussusceptions decreased from 190 cases (6.5 cases/10 000 infants) in 1989 to 98 cases (3.9 cases/10 000 infants)
in 1998 (
METHODS
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Methods
Results
Discussion
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2
test.9 Odds ratios with Fisher's exact test were used as
a measure of association between surgical procedure and potential risk
factors,10 including patient demographics (age, sex, race)
and insurance provider.
RESULTS
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Abstract
Methods
Results
Discussion
References
2 test for trend, P < .001), for an average annual rate of 5.4 per 10 000 (Fig
1). Over the same period, the percentage of patients having surgical resections decreased from 13% in 1989 to
9% in 1998.
View larger version (29K):
[in a new window]
Fig. 1.
Number of hospitalizations by surgical procedure and incidence of
intussusception-associated hospitalizations for children <1 year old,
New York State, 1989-1998.
The age distribution of hospitalizations for intussusception was
examined for all infants <1 year old (Fig
2). Intussusception-related hospitalizations were rare among children in the first few months of
life, peaked among infants 4 to 10 months old, and declined thereafter.
Twenty-three percent of patients with rotavirus-associated cases and
26% of all patients with diarrhea were admitted to hospitals during
their first 3 months of life, compared with 6% of patients with
intussusception. The characteristics of patients with rotavirus diarrhea were compared with those who had intussusception that was
treated medically or surgically (Table
1). Overall, 61% of the infants having
intussusception were 6 months of age or older, 61% were male, 49%
were white, 42% had private insurance, and 55% were hospitalized for
3 days or more, and their median hospital cost was $3461. Patients who
had surgery with resection were younger, were more likely to have
private insurance and a longer length of stay, and incurred greater
direct medical costs ($8877) than those who did not need surgery
($1751) or those who had only a simple reduction without resection
($5417). By contrast, the 2336 patients with rotavirus diarrhea coded
on their hospital discharge chart were younger (43% <6 months), more
likely to be white (64%) and female (44%), and had a longer length of
stay (
3 days, 68%) but a lower median cost of care ($2952) compared with patients who had intussusception.
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To examine the possible association of intussusception and natural rotavirus infection, the monthly numbers of hospitalizations for diarrhea and intussusception were compared for the full 10-year period, and data for rotavirus diarrhea were included from 1993, when the ICD-9-CM code was first introduced (Fig 3). The marked winter peaks and summer troughs of rotavirus hospitalizations, which were clearly reflected in the total diarrhea hospitalization data, were not observed for intussusception.
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A total of 92 196 doses of rotavirus vaccine were distributed to individual physicians and group practices and 17 484 doses distributed to pharmaceutical wholesalers, drug warehouses, and distribution warehouses in New York during the 9 months of the rotavirus vaccination program (October 1998 through June 1999). A total of 21 561 doses were returned to Wyeth Laboratories, Inc. Assuming that 60% of the distributed vaccine was used as first doses, an estimated 21% of children in New York received this vaccine. Because preliminary analyses showed that the rotavirus vaccine was associated with significant excess risk of intussusception in the week after vaccination,5 we looked for excess cases that would have occurred during the 9 months of the rotavirus vaccination program compared with the same period during the preceding year. A total of 81 cases occurred during the vaccination period, compared with 78 during the prevaccination period, an observed difference of only 3 cases. Among the approximately 248 700 newborns in New York in 1998, an estimated 52 000 received 1 or more doses of vaccine. If the risk of excess intussusception from the vaccine was 1.8 compared with those who were never vaccinated, based on 1998 intussusception incidence rate (3.9 per 10 000 infants), we would have expected an excess of about 12 intussusception cases attributable to the vaccine during this period, a number substantially greater than that observed. However, if the vaccine-attributable risk were 1 in 12 000, as indicated by the most recent estimate from the cohort study conducted by the CDC,11 the number estimated would not differ significantly from the number we observed. The medical charts of 20 cases from New York State excluding New York City were reviewed by immunization staff of the New York State Department of Health, and vaccine histories were obtained from their health care providers (Table 2). Five patients had received rotavirus vaccine: 3 had 3 doses, 1 had 2 doses, and 1 had 1 dose. All 5 patients were hospitalized for intussusception after the first dose of vaccine: 2 patients within 1 week after the first dose (day 5 and day 6) and the others on days 9, 12, and 57. Overall, 5 vaccinees were admitted to hospitals before 7 months of age, 2 were males, all were white, and all had private health insurance. In comparison, the 15 who had not received rotavirus vaccine were older (33% were admitted before 7 months of age, P = .02) and were more likely to be male (80%, P = .13) and nonwhite (33.%, P = .19) and did not have private health insurance (47%, P = .08). The characteristics of patients who were not vaccinated were similar to those of all infants hospitalized for intussusception. The median length of hospital stay was 3 days for both vaccinated and unvaccinated patients, and the median hospital direct cost was lower for vaccinated patients than for unvaccinated patients and for all intussusception-associated hospitalizations. Surgery was not associated with the use of rotavirus vaccine.
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DISCUSSION |
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This study provides new insights into the epidemiology of intussusception in children and approach to assess the impact of the attributable risk of intussusception associated with the rotavirus vaccine. Of note, the annual incidence of intussusception among infants in New York State declined continuously between 1989 and 1998, from 6.5 to 3.9 cases per 10 000 children, and this decline was accompanied by a decrease in the percentage of children who needed surgery (54% to 46%). This change could result from either a true decrease in incidence or an increase in the outpatient management of this disease, with a shift from hospitalizations to treatment in short-stay beds and holding areas, which are not counted as true hospital admissions. Early cases of intussusception can now be detected by sonogram and reduced with an air or barium enema,12-15 outpatient procedures that could reduce hospitalizations and would not be reported in our dataset. Because New York State has complete statewide hospitalization data readily available, CDC has used New York State incidence data as a baseline to assess the attributable risk of intussusception from the vaccine in the United States.6 With the lower current baseline risk, the excess number of intussusception cases attributed to the vaccine nationally would be reduced substantially.
Monthly figures for intussusception monitored over 10 years indicated no seasonal trends over time and no correlation with diarrhea or rotavirus hospitalizations, both of which demonstrate a marked winter peak, reflecting this characteristic of rotavirus epidemiology. Although this observation does not rule out a causal association of intussusception with natural rotavirus infection, it suggests that any such association must be small and, if true, rotavirus could account for only the small fraction of intussusception cases that occur during the peak rotavirus season (February through April).
This study provides some clues, but no clear answers, about the excess risk of intussusception associated with the rotavirus vaccine. On one hand, the number of cases of intussusception in the 9-month vaccination period (n = 81) did not differ significantly from the 78 cases in the same period during the preceding year. This similarity suggests that the excess risk of vaccine-associated intussusception is small. The original estimate of the association suggested an odds ratio of 1.8 excess cases among the vaccinated versus never vaccinated, a figure that in New York would have resulted in 12 excess cases, substantially more than the 3 excess cases we observed. The more recent and lower estimate of 1 excess case in 12 000 infants immunized would lead to 5 cases, a number within the range of variability of our observed figures. However, data on the histories of rotavirus immunization of all intussusception cases that occurred during the period of the vaccination program were not obtained and would necessitate a separate study. Of the 20 cases reviewed as a subset, 5 patients received rotavirus vaccine and, of these, 2 developed intussusception in the week after rotavirus vaccination.
Although the small increase in the number of intussusception cases observed does not suggest a highly elevated risk associated with receipt of the vaccine, the numbers are too small to adequately assess a lesser risk of intussusception from the vaccine. First, none of the intussusception cases in the dataset were confirmed through chart review; we may have systematically overestimated the true number of cases if some of the diagnoses coded on the record were not confirmed in the chart. We may have underestimated the true number of cases by not counting patients treated in an outpatient or short-stay setting. Furthermore, the number of children estimated to have received at least 1 dose of rotavirus vaccine, 52 000 or 21% of the birth cohort, is a best guess based on the number of doses of vaccine distributed in the state (N = 88 119). Both of these deficiencies could be corrected by conducting a larger-scale study and assessing in full the impact of the vaccine in the state. A follow-up of the full cohort could provide more accurate data on the exact risk attributable to the vaccine in a single large state.
Two prominent epidemiologic features of intussusception observed in this study have been seen in every previous study and remain unexplained. The first is the peculiar age distribution, with few cases among infants in the first 2 to 3 months of life and a decline after the first year, a pattern seen for many childhood infectious diseases.16,17 The protection conferred in the neonatal and postneonatal period may result from maternal antibodies or the lack of maturation of germinal centers in the Peyer's patches of the terminal ileum, a recognized leading edge for intussusception events. If maternal antibody were key, one might expect that cases observed in neonates might preferentially affect premature infants with low levels of maternal antibody or might result from anatomic problems (eg, polyps, diverticula), a hypothesis that could be tested by case investigation. A second feature is the marked predilection of intussusception for boys, a disparity observed in other congenital anomalies of the gastrointestinal tract (eg, pyloric stenosis, duodenal atresia).
Although our understanding of the pathogenesis of intussusception remains incomplete, the incidence, the need for surgery, and the mortality from the disease have all declined over time. In New York, case fatality has declined to 1 death per 475 cases, and recent studies suggest that the need for surgery and the risk of death can be decreased by shortening the period between symptom onset, diagnosis, and treatment.18 Given the increased awareness of intussusception caused by the rotavirus vaccine, physicians may learn to make an earlier diagnosis and send the patient for treatment sooner, leading to improvements in outcome. Estimation of the exact risk of intussusception attributable to the rotavirus vaccine is important to more fully understanding the epidemiology of this condition and to further develop rotavirus vaccines. The study initiated in New York should be repeated in other states with large populations of immunized children to assess a larger cohort and identify the true risk of intussusception in populations for which full data on hospitalizations are available. At the same time, the benefits of the vaccine, measured as a decline in winter hospitalizations among children in the cohort who received the vaccine, could be assessed to give health care decision makers a balanced view of risks and benefits.
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ACKNOWLEDGMENTS |
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We thank John O'Connor for editorial assistance in preparing this manuscript, and Drs Ben Schwartz, Robert Chen (NIP data), and Michael Blum (Wyeth data) for technical assistance.
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FOOTNOTES |
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A preliminary version of this paper was presented at the International Conference on Emerging Infectious Diseases; July 16-19, 2000; Atlanta, GA (Abstract 20469).
Received for publication Sep 5, 2000; accepted Nov 1, 2000.
Reprint requests to (H.-G.C.) New York State Department of Health, Room 1143, Corning Tower Building, Empire State Plaza, Albany, NY 12237. E-mail: hgc04{at}health.state.ny.us
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ABBREVIATIONS |
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CDC, Centers for Disease Control and Prevention; NIP, National Immunization Program; SPARCS, Statewide Planning and Research Cooperative System; ICD-9-CM, International Classification of Diseases, 9th Revision, Clinical Modification..
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