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Pediatric Infectious Disease Journal:
doi: 10.1097/INF.0b013e318275328f
Vaccine Reports

Effectiveness of an Incomplete RotaTeq (RV5) Vaccination Regimen in Preventing Rotavirus Gastroenteritis in the United States

Wang, Florence T. ScD*; Mast, T. Christopher PhD; Glass, Roberta J. MS*; Loughlin, Jeanne MS*; Seeger, John D. PharmD, DrPH*‡

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Author Information

From the *OptumInsight Epidemiology, Waltham, MA; Merck Research Laboratories, North Wales, PA; and Harvard Medical School and Harvard School of Public Health, Boston, MA.

Accepted for publication September 19, 2012.

OptumInsight has one ongoing study for a product unrelated to RotaTeq (RV5) that is funded by a research contract between OptumInsight Epidemiology and Merck & Co., Inc. This contract encompasses all aspects of the study including study design and execution, analysis, reporting of results and writing of articles. The contract grants OptumInsight Epidemiology oversight of the study conduct, reporting and interpretation, as well as final wording of any resulting articles. T.C.M. is an employee of Merck & Co., Inc. The authors have no other funding or conflicts of interest to disclose.

Address for correspondence: John D. Seeger, PharmD, DrPH, OptumInsight Epidemiology, 950 Winter Street, Suite 3800, Waltham, MA 02451. E-mail: jdseeger@partners.org.

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Abstract

Background: Effectiveness of the pentavalent rotavirus vaccine (RV5) after administration of the complete (3 dose) regimen has been demonstrated in a real-world setting. This study assessed the effectiveness of RV5 following partial completion of the 3-dose regimen.

Methods: Using a large national health insurance claims database, 2 cohorts of infants (those who received RV5 and a concurrent group who received diphtheria-tetanus-acellular pertussis, but not RV5) were followed through the 2007 and 2008 rotavirus seasons (January 1 to May 31) to identify cases of rotavirus gastroenteritis and all-cause gastroenteritis resulting in medical care encounters. Vaccine effectiveness following the first and the second RV5 doses was estimated by quantifying reductions in hospitalizations, emergency department (ED) and physician office visits.

Results: A first RV5 dose was received by 42,306 infants whereas 28,417 infants in the concurrent comparison group received a first diphtheria-tetanus-acellular pertussis dose; 43,704 infants received a second RV5 dose, and 31,810 infants received a second diphtheria-tetanus-acellular pertussis dose. One dose of RV5 was associated with 88% effectiveness against rotavirus gastroenteritis hospitalizations and ED visits and 44% effectiveness against all-cause gastroenteritis hospitalizations and ED visits. A 2-dose regimen of RV5 was associated with 94% effectiveness against rotavirus gastroenteritis hospitalizations and ED visits and 40% effectiveness against all-cause gastroenteritis hospitalizations and ED visits.

Conclusion: The RV5 vaccine exhibits effectiveness against rotavirus gastroenteritis even before completing the full 3-dose regimen. These results are of particular relevance when considering the benefits of a partially completed rotavirus vaccine series.

Rotavirus is the most common cause of severe pediatric gastroenteritis, with most children having been infected by age 5. Before the introduction of the pentavalent vaccine, over 100 million cases of gastroenteritis and over 400,000 deaths each year among children aged <5 years were attributed to rotavirus worldwide.1 In the United States, rotavirus was associated with approximately 350,000 hospitalizations and emergency department (ED) visits, resulting in a total annual societal cost of almost $1 billion.2–4

RotaTeq (Merck & Co Inc, Whitehouse Station, NJ), an oral pentavalent rotavirus vaccine (RV5), was first available in the United States in February 2006 and was subsequently recommended for routine use by the Advisory Committee on Immunization Practices.4 The vaccine is indicated for the prevention of rotavirus gastroenteritis (RGE) caused by serotypes G1–G4, which account for approximately 90% of all RGE in the United States.5,6 The RV5 series consists of 3 doses administered orally starting at 6–12 weeks of age, with the subsequent doses administered at 4-week to 10-week intervals. The third dose should be given by 32 weeks of age.7 The label-recommended schedule corresponds to the standard pediatric visit schedule.

In prelicensure clinical trials, the vaccine was efficacious with respect to the prevention of RGE. The vaccine reduced the incidence of G1–G4 RGE hospitalization and ED care by 95% (95% confidence interval [CI]: 91%–97%), and was associated with an 86% reduction in clinic visits for G1–G4 RGE (95% CI: 74%–93%).8 Recent studies in the postmarketing setting reported the complete RV5 vaccination series to be effective in preventing RGE and all-cause gastroenteritis (AGE), with magnitude of vaccine effect similar to that observed in the efficacy trials.9–11 Further, these studies demonstrate that RV5 was associated with a substantial reduction in RGE and AGE-related hospitalizations and ED visit days and associated cost.

No US national data are available on whether an incomplete regimen (<3 doses) of RV5 confers protection in the real-world setting. To evaluate this, we describe the occurrence of RGE and AGE during the 2007 and 2008 US rotavirus seasons among infants after receipt of 1 dose or 2 doses of RV5, and compared it to that of infants after receipt of 1 dose or 2 doses of diphtheria-tetanus-acellular pertussis (DTaP) among those who did not receive RV5. As RV5 was introduced in 2006 for routine use and was the only marketed rotavirus vaccine in the United States through the 2008 season, coverage of the vaccine was not immediately widespread, offering a natural opportunity to compare RV5-vaccinated and unvaccinated infants in a concurrent manner.

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PATIENTS AND METHODS

Data Source

This observational study used health insurance claims data from a proprietary research database built from electronically captured provider, facility and pharmacy claims of a large US health insurer. The individuals covered by this health insurance are geographically diverse across the United States. Fully insured coverage minus applicable copays for medical and prescription drug services is provided. The clinicians or institutions providing these services submit their claims for payment directly to the health insurer. Data derived from these claims may be used for research following approval by an appropriate institutional review board, and all data access conforms to applicable Health Insurance Portability and Accountability Act policies, which establish the minimum US Federal standards for protecting the privacy of protected health information.

There was no active enrollment or active follow-up of children, and no data were directly collected from parents or infants. The Privacy Board of the New England Institutional Review Board approved this study.

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Study Population

All infants who were enrolled in the health plan within 1 week of birth (to address the potential of missing claims for early vaccine doses) and vaccinated at <10 months of age in the course of ordinary clinical practice with their first dose of RV5 or DTaP (but not RV5) from February 2006 through December 2007 were eligible for inclusion in the study. DTaP recipients (concurrent DTaP cohort) were chosen as comparators because the recommended ages for receiving the first doses of DTaP (ages 2, 4, 6 months) are similar to those of RV5. To address the concern in the first year of availability that infants receiving a first dose of RV5 might be older than those receiving a first dose of DTaP, RV5 and DTaP recipients were matched (1:2) on age at first dose. All infants first vaccinated with RV5 and DTaP in 2007 were included.

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Identification of RV5 and DTaP Vaccinations

Vaccinations were identified by the presence of Current Procedural Terminology classification codes or National Drug Codes on health insurance claims: RV5 (Current Procedural Terminology 90680; National Drug Codes 00006-4047-31 or 00006-4047-4); DTaP (Current Procedural Terminology 90698, 90700, 90721 or 90723). For each vaccine type, the dates of the vaccination claims determined the relative sequence of a dose in a vaccine series (ie, the earliest dose was dose 1).

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Identification of Outcomes

The insurance claims histories of vaccinated infants in the study population were followed through the 2007 and 2008 rotavirus seasons to identify claims of RGE and AGE. The rotavirus season duration was defined as January 1 through May 31. This is consistent with the annual unimodal distribution of positive rotavirus tests in the United States.12 Follow-up began on the later of 14 days after the receipt of the first or second RV5 or DTaP dose, or the start of the season. The 14-day lag in the start of follow-up allowed for sufficient time to establish a vaccine immune response, and corresponds to the design of the prelicensure trials.8 All infants who received a dose were included in the analysis for 1 dose, regardless of receipt of subsequent doses, with follow-up ending upon the earlier of the infant’s receipt of a successive dose of the same vaccine, the infant’s disenrollment from the insurance plan, the infant reaching 1 year of age or the end of the season. This analysis therefore included those infants who received only 1 dose, only 2 doses and those who received all 3 doses. Likewise, the 2-dose analysis included infants who received only 2 doses and those who received 3 doses, with follow-up ending upon the earlier of either the infant’s receipt of a third dose of the same vaccine, the infant’s disenrollment from the insurance plan, the infant reaching 1 year of age or the end of the season. Follow-up for infants in the concurrent DTaP cohort was censored upon receipt of RV5.

Both of the complementary outcomes (RGE and AGE) were evaluated by using International Classification of Diseases, Ninth Revision (ICD-9) diagnosis codes associated with a hospitalization, ED or outpatient visit: RGE (008.61) and AGE (001–005 excluding 003.2, 006–007 excluding 006.2–006.6, 008.0–008.8 [including RGE], 009.0–009.3 and 558.9). To increase the likelihood that the predominant reason for identified health visits was related to the study outcomes, only the diagnostic codes recorded in the first position of the claim forms submitted for medical services were included in the analysis. For hospitalization-associated claims, the primary diagnostic code corresponds to the hospital discharge diagnosis. The date of the diagnosis-associated claim served as a proxy for the diagnosis date. Cases of each outcome were tabulated by site of medical care: outpatient versus ED and hospitalization combined. For each type of site, 2 successive claims associated with each outcome were counted as 2 separate events if a 14-day or greater gap existed between the diagnosis dates.

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Statistical Analysis

The RV5 and DTaP cohorts were described with respect to baseline characteristics. To assess potential differential resource utilization between the 2 cohorts, the prevalence of healthcare claims for otitis media and dermatitis, proxies for infantile healthcare utilization unrelated to rotavirus, identified from birth through the receipt of the corresponding vaccine dose among the RV5 infants was compared with that of the DTaP infants.

The incidence of RGE and AGE after a first dose of RV5 was compared with the incidence after a first dose of DTaP in the combined hospital and ED setting, and in the outpatient setting. For each combination of health outcome and site of care, we fitted multivariable Poisson regression models of the average count of each outcome, in which we included terms for age at diagnosis (<5 months, 5–8 months, 9+ months), sex and rotavirus season (2007 or 2008) where the number of outcomes permitted such stratification. Vaccine effectiveness (VE) was defined as 1 minus the rate ratio comparing infants receiving RV5 to infants receiving DTaP, and corresponding asymptotic 95% CI were estimated.13 A supplementary analysis that included RGE and AGE codes identified from all coding positions was conducted, as was an exploratory analysis restricted to those who received only 1 dose of their respective vaccines. Similar comparisons were conducted among infants who received 2 doses of RV5 with those with who received 2 doses of DTaP.

All analyses were conducted using SAS version 9.1 (SAS Institute Inc., Cary, NC) and STATA version 9 (StataCorp, College Station, TX).

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RESULTS

The analyses included 42,306 infants who received at least 1 dose of RV5 and 28,417 infants who received at least 1 dose of DTaP from February 2006 through December 2007, and 43,704 infants who received at least 2 doses of RV5 and 31,810 infants who received at least 2 doses of DTaP (Tables 1 and 2). The cohorts of RV5 infants were comparable to the DTaP infants with respect to age, sex, regional differences and prevalence of otitis media and dermatitis before receiving their respective first and second vaccine doses. Even without age-matching, infants first vaccinated with RV5 in 2007 were similar in age to those vaccinated with DTaP. Within both cohorts, the majority of infants received 3 doses of the corresponding vaccine. The average length of follow-up for the RV5 and DTaP infants were similar in the 1 dose (6 weeks) and 2 doses (7 weeks) analyses, reflecting the recommended dosing schedule of the vaccines.

Table 1
Table 1
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Table 2
Table 2
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Over the 2007 and 2008 rotavirus seasons, 1 dose of RV5 was associated with an 88% VE against RGE hospitalizations and ED visits combined (95% CI: 45%–99%; Table 3). The magnitudes of VE were similar when the analysis was restricted to infants who received only 1 dose of their respective vaccines (ie, did not receive a subsequent dose) (VE: 84%, 95% CI: <0%–99%). In the outpatient setting, VE against RGE was 100% (95% CI: 54%–100%). Results of analyses restricted to infants who received only 1 dose of their respective vaccines were again similar. In a supplementary analysis, we expanded the outcome definition to diagnostic codes recorded in all positions of the claims; VE was somewhat lower for both the combined hospitalization and ED setting (VE: 78%, 95% CI: 27%–95%) and the outpatient setting (VE: 73%, 95% CI: 8%–94%). Adjusted estimates of VE for RGE were not calculated because of the small number of events among the infants receiving RV5.

Table 3
Table 3
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One dose of RV5 was associated with a 44% VE against AGE identified in the combined hospitalization and ED setting (95% CI: 18%–62%; Table 2). The VE was somewhat higher among those who received only 1 dose of their respective vaccines (VE: 67%, 95% CI: 34%–84%). The regression result adjusted for age was similar (VE: 42%, 95% CI: 16%–60%), as was the result adjusted for sex and calendar year. In the outpatient setting, VE against AGE was 17% (95% CI: 6%–23%). The sex-adjusted and calendar-adjusted VE estimate was also similar, as was the adjusted estimate accounting for age, sex and rotavirus season (VE: 13%, 95% CI: 2%–23%), as were the results of analyses restricted to infants who received only 1 dose of their respective vaccines.

In the same period, 2 doses of RV5 was associated with a 94% VE against RGE hospitalizations and ED visits combined (95% CI: 61%–100%; Table 4). The magnitudes of VE were similar when the analysis was limited to those who received only 2 doses of their respective vaccines (VE: 100%, 95% CI: <0%–99%). In the outpatient setting, VE against RGE was 40%, although the CI included zero. In a supplementary analysis that expanded the outcome definition to include diagnosis codes in any claim position (not just the primary), the VE remained similar for both the combined hospitalization and ED setting (VE: 94%, 95% CI: 61%–100%) and the outpatient setting (VE: 40%, 95% CI: <0%–88%). Adjusted estimates of VE for RGE were not calculated because of the small number of events among the infants receiving RV5.

Table 4
Table 4
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The VE associated with 2 doses of RV5 against AGE identified in the combined hospitalization and ED setting was 40% (95% CI: 18%–56%; Table 3). The regression result adjusted for age was similar (VE: 37%, 95% CI: 16%–53%), as was the result adjusted for sex and calendar year. In the outpatient setting, VE against AGE was 31% (95% CI: 24%–38%). The sex-adjusted and calendar year–adjusted VE estimate was also similar, as was the adjusted estimate accounting for age, sex and rotavirus season (VE: 26%, 95% CI: 18%–33%), as were the results restricted to infants who received only 2 doses of their respective vaccines.

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DISCUSSION

In this large, nationwide, observational study, an incomplete RV5 regimen consisting of a first or first and second dose was found to be effective in preventing rotavirus gastroenteritis through the 2007 to 2008 rotavirus seasons. Our study yielded estimates of vaccine effectiveness that were similar to those of prelicensure clinical trials and postmarketing effectiveness studies.8–11 In a post hoc analysis of a clinical trial, efficacy between doses 1 and 2 was estimated at 82% whereas efficacy between doses 2 and 3 was estimated at 84% (compared to our findings for RGE of 88% and 94%, respectively).14 A hospital-based case-control study with laboratory testing for rotavirus reported VE against hospital or ED RGE of 69% for 1 dose and 81% for 2 doses of RV5.10 The broad representativeness of our large, underlying database population increases the likelihood that these results are generalizable to real-world scenarios where infants may inadvertently not complete the recommended RV5 vaccination series. Although the approved indication of the vaccine is 3 doses, multiple factors could contribute to an infant not completing a vaccine regimen. Therefore, these results are of particular relevance to healthcare professionals when assessing the impact of a partially completed RV5 series.

The majority of infants in both cohorts received 3 doses of their corresponding cohort vaccine in accordance with the recommended vaccine schedule, with an average length of 6 weeks between the first and the second dose, and an average length of 7 weeks between the second and the third dose. Thus, the estimates of effectiveness most directly reflect short-term protection. In an exploratory analysis restricted to infants who received only 1 dose (average follow-up for RV5 infants: 14.8 weeks) and those who received only 2 doses (average follow-up for RV5 infants: 12.6 weeks), we found similar trends of vaccine effectiveness for rotavirus gastroenteritis as the main analysis. Although the exploratory analysis results may be biased as it is conditioned on the infants not receiving any other doses, the results do provide some reassurance that the short-term protection is sustained beyond the 6-week period.

In this study, we assessed VE during the 5 months of the RV season because such estimates are likely to have the most public health relevance with regards to assessing impact of vaccination on disease burden. As there may be differences in VE during rotavirus seasons of varying severity, it would be of interest to assess potential differences in VE between the 2 rotavirus seasons in our study, as the US 2008 season was milder than previous seasons, as measured by RGE incidence. Unfortunately, we were not able to report separate VE estimates for each of the season because of the small number of cases among the RV5-vaccinated cohort in 2008.

Although there are 2 rotavirus vaccines currently licensed in the United States (RV5 [RotaTeq] and RV1 [Rotarix, GlaxoSmithKline Biologicals, Rixensart, Belgium]), misclassification of rotavirus vaccine dose because of mixed vaccination schedules (infants receiving RV1 instead of RV5) in the study is unlikely. Our study accrued infants who received a first dose from February 2006 through December 2007, with follow-up until May 2008. Since RV1 was approved in April 2008 and not marketed until August 2008,15 RV5 was the sole rotavirus vaccine marketed in the United States throughout the study period.

The observed VE against AGE hospitalizations and ED visits combined was somewhat higher than VE against the same outcomes when they are observed in the outpatient setting. This is consistent with the observed higher efficacy in clinical trials for more severe disease.14,16 In addition, these results may be indicative of greater precision in the use of diagnosis codes for RGE and AGE in the hospital or ED setting compared to the outpatient setting.17

Although relatively few cases of RGE were identified by the ICD-9 diagnosis code for rotavirus, the identified cases are highly likely to be actual RGE cases given that this code is reported to have high positive predictive value, albeit low sensitivity. Hsu et al18 found although 98% of patients with a rotavirus-associated discharge code were confirmed to be rotavirus positive by laboratory testing, only 25% with rotavirus-positive tests were assigned a rotavirus code. Hence, the reported RGE incidence relying solely on this code is likely to be substantially underestimated in this study.

In the absence of laboratory confirmation, epidemiologic studies commonly identify RGE through hospital discharge data by ICD-9 diagnosis codes for AGE that capture diarrhea of determined and undetermined etiology.18,19 It has been reported that 52% of children <5 years of age with a hospital discharge diagnosis of AGE tested positive for rotavirus,18 and that a higher proportion of AGE in children less than age 5 years is related to the rotavirus in the winter months of January through May.19 Thus, by evaluating the incidence of AGE during only the rotavirus seasons, this study increased the concordance between AGE diagnoses and RGE, although AGE incidence as identified in this study is expected to lack some sensitivity as a measure of RV5 VE because some portion of AGE is unrelated to rotavirus.

In this study, the main analysis identified health outcomes through diagnosis codes recorded in the primary position. Although this improved the probability that the study-outcome variables captured only RGE and AGE events, we note that some study outcomes were not counted as the ICD-9 code was recorded in a nonprimary position. This may have led to an underestimated incidence rate, but it is unlikely to have affected our measures of vaccine effectiveness, unless RV5 recipients had a different concordance between the claim code position and the underlying clinical diagnosis from DTaP recipients. As a demonstration of this point, our secondary analyses using codes in any position yielded similar vaccine effectiveness estimates.

Because of these factors, we note that there is likely incomplete ascertainment of both all-cause gastroenteritis and rotavirus gastroenteritis cases within our study, resulting in a lower absolute incidence than actually present in the population. However, the measure of vaccine effectiveness is a relative one, so it will be much less affected by incomplete ascertainment of gastroenteritis with corresponding underestimation of absolute incidence, unless the incomplete ascertainment is substantially different among RV5-exposed infants. For example, if physicians preferentially do not diagnose RGE among RV5 recipients, our measures of VE would be overestimates. For the hospitalized and ED-treated cases, treating physicians are likely unaware of the RV5 vaccination status of the infants. Indeed, the estimates of vaccine effectiveness in this study are similar to those of a prelicensure clinical trial and postmarketing effectiveness studies, external comparisons that suggest a lack of substantial bias in the estimates obtained in this study.10,11,14

There are limitations associated with the use of claims data for healthcare research. Misclassification of exposure is a possibility if all vaccination doses were not captured in the claims database. In this circumstance, estimates of vaccine effectiveness may have been inflated if RV5 doses were missed. However, the similarities of VE estimates in this study compared with other reports provide further assurance that the RGE VE estimates are relatively unbiased.10,14 The diagnosis code on a medical claim may not be definitive because the code may represent a rule-out diagnosis, or may be incorrectly recorded. Diagnosis of RGE requires laboratory confirmation, and laboratory results were not available for this study. Because insurance claims represent financial transactions that translate into reimbursement for providers, a financial incentive exists for providers and insurers to record them correctly, so the billable medical services represented in the database (both vaccine exposure and study outcomes) are likely to be complete.

Finally, measures of association should be interpreted with caution as there may be unmeasured factors associated with both RV5 administration and gastroenteritis, which were not taken into account in the analyses and may bias the observed measures. Because the early differential in RV5 uptake was likely based on provider and governmental characteristics such as initial vaccine availability and state purchasing patterns rather than patient characteristics, we were able to construct a relatively comparable comparison group for the evaluation of effectiveness. As infants were members of the same commercial health plan, they likely had similar socioeconomic backgrounds. There were no substantial demographic differences between the 2 cohorts, and both had similar baseline clinical features, reflecting comparability of healthcare access and utilization. Therefore, the compared groups should have similar exposure to the rotavirus and underlying risk for RGE. Overall, crude and adjusted estimates of VE were similar, suggesting that strong confounding from an unmeasured source is unlikely.

In summary, an incomplete RV5 vaccination regimen was associated with lower incidence of RGE and AGE through the rotavirus seasons. Further research is needed to assess whether the reported magnitude of VE with 1 or 2 RV5 doses is observed in other populations or healthcare settings.

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ACKNOWLEDGEMENT

All authors fulfilled the conditions of authorship and have approved the article as submitted.

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REFERENCES

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9. Wang FT, Mast TC, Glass RJ, et al. Effectiveness of the pentavalent rotavirus vaccine in preventing gastroenteritis in the United States. Pediatrics. 2010;125:e208–e213

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12. Centers for Disease Control and Prevention (CDC). . Delayed onset and diminished magnitude of rotavirus activity–United States, November 2007-May 2008 MMWR Morb Mortal Wkly Rep. 2008;57:697–700

13. Ewell M. Comparing methods for calculating confidence intervals for vaccine efficacy. Stat Med. 1996;15:2379–2392

14. Dennehy PH, Vesikari T, Matson DO, et al. Efficacy of the pentavalent rotavirus vaccine, RotaTeq® (RV5), between doses of a 3-dose series and with less than 3 doses (incomplete regimen). Hum Vaccin. 2011;7:563–568

15. Rotarix® [prescribing information]. 2011 Rixensart, Belgium GlaxoSmithKline Biologicals

16. Vesikari T, Karvonen A, Prymula R, et al. Efficacy of human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in European infants: randomised, double-blind controlled study. Lancet. 2007;370:1757–1763

17. Mast TC, Walter EB, Bulotsky M, et al. Burden of childhood rotavirus disease on health systems in the United States. Pediatr Infect Dis J. 2010;29:e19–e25

18. Hsu VP, Staat MA, Roberts N, et al. Use of active surveillance to validate international classification of diseases code estimates of rotavirus hospitalizations in children. Pediatrics. 2005;115:78–82

19. Patel MM, Tate JE, Selvarangan R, et al. Routine laboratory testing data for surveillance of rotavirus hospitalizations to evaluate the impact of vaccination. Pediatr Infect Dis J. 2007;26:914–919

rotavirus; vaccines; gastroenteritis; immunization

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