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Pediatric Infectious Disease Journal:
doi: 10.1097/INF.0b013e3181fefdc0
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Uptake, Impact, and Effectiveness of Rotavirus Vaccination in the United States: Review of the First 3 Years of Postlicensure Data

Tate, Jacqueline E. PhD; Cortese, Margaret M. MD; Payne, Daniel C. PhD; Curns, Aaron T. MPH; Yen, Catherine MD, MPH; Esposito, Douglas H. MD; Cortes, Jennifer E. MD; Lopman, Benjamin A. PhD; Patel, Manish M. MSc, MD; Gentsch, Jon R. PhD; Parashar, Umesh D. MB BS, MPH

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Author Information

From the Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, GA.

Accepted for publication September 28, 2010.

The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention (CDC).

Address for correspondence: Jacqueline E. Tate, PhD, Centers for Disease Control and Prevention, 1600 Clifton Road NE, MS-A47, Atlanta, GA 30333. E-mail: jqt8@cdc.gov.

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Abstract

Background: Rotavirus vaccine was recommended for routine use in US infants in 2006. Before the introduction of vaccine, rotavirus was the most common cause of severe gastroenteritis in children <5 years of age in the United States.

Methods: We reviewed published data to summarize the US experience during the first 3 years of its rotavirus vaccination program.

Results: Rotavirus seasons have been delayed and diminished in magnitude during the postvaccine era compared with the prevaccine era. Hospitalizations, emergency department visits, and outpatient visits due to gastroenteritis have declined dramatically in children <5 years of age including in children age-ineligible to have received vaccine, suggesting indirect benefits of vaccination. Rotavirus vaccine has been widely accepted by pediatricians. Vaccine coverage is steadily increasing but remains lower than coverage levels of other routine infant immunizations.

Conclusions: The implementation of routine childhood immunization against rotavirus has rapidly and dramatically reduced the large health burden of rotavirus gastroenteritis in US children. Continued monitoring of rotavirus diarrhea is needed to determine if immunity wanes as vaccinated children get older and to better quantify the indirect benefits of vaccination. Ongoing surveillance will also enable monitoring of the long-term impact of vaccination on rotavirus epidemiology.

Before the introduction of rotavirus vaccine in the United States in 2006, rotavirus was the most common cause of severe gastroenteritis in children <5 years of age in the United States.1–5 Although mortality due to rotavirus was uncommon, with an estimated 20 to 60 deaths annually, rotavirus gastroenteritis resulted in 55,000 to 70,000 hospitalizations, 200,000 emergency department (ED) visits, and 400,000 outpatient visits each year among US children <5 years of age.6,7 This morbidity created a substantial economic burden, with direct medical costs of $300 million annually, and total costs of more than 1 billion dollars when indirect costs including lost wages were added.7

In February 2006, the Advisory Committee on Immunization Practices (ACIP) recommended the routine use of pentavalent rotavirus vaccine (RV5; RotaTeq, Merck and Co.) in US infants with 3 doses administered orally at 2, 4, and 6 months of age.8 In June 2008, ACIP updated its rotavirus vaccination recommendations to introduce use of the monovalent rotavirus vaccine (RV1; Rotarix, GSK Biologicals).9 RV1 is a 2 dose vaccine administered orally at 2 and 4 months of age.

In this report, we summarize published data on the US experience during the first 3 years of its rotavirus vaccination program. We provide information on acceptance of the vaccine by US physicians, adherence to age recommendations for administration, vaccine uptake and coverage, effectiveness of the vaccine under conditions of routine use, and the impact of the vaccine on disease trends.

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VACCINE ACCEPTANCE AND USE BY US PHYSICIANS

In 1999, the first rotavirus vaccine (RotaShield, Wyeth-Lederle Vaccines) licensed and recommended for use in the United States was withdrawn from the market less than 1 year after its introduction because of an association with intussusception, a condition in which a portion of the bowel telescopes into another, resulting in potential bowel obstruction, perforation, and/or necrosis.10,11 Because of this previous experience with RotaShield, understanding the concerns and barriers associated with the use of the newly recommended rotavirus vaccines is important to help ensure that these new vaccines are used to their fullest potential.

Approximately 18 months after the 2006 ACIP recommendation, a national survey showed that acceptance of the new rotavirus vaccine by pediatricians was high, with 88% agreeing somewhat or strongly that the vaccine should be routinely administered to all infants and 85% reporting that they routinely administered rotavirus vaccine to eligible infants in their practice.12 The perceived need and use of rotavirus vaccine was lower among family practice physicians, with 64% agreeing somewhat or strongly that the vaccine should be routinely administered to all infants and only 45% reporting that they routinely administered rotavirus vaccine to eligible infants in their practice.12 Financial concerns, including cost of purchasing vaccine, lack of adequate reimbursement, and lack of coverage by insurance companies, were commonly identified as barriers to vaccine use by both pediatricians and family practice physicians, but family practice physicians also had more concerns regarding vaccine safety and the burden imposed by adding another vaccine to the immunization schedule.12 The anticipated vaccine use and perceived barriers to use in this study are consistent with additional assessments conducted both pre- and postvaccine introduction in the United States.13–15

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ADHERENCE TO GUIDELINES ON AGE AT ADMINISTRATION OF ROTAVIRUS VACCINES

The newly introduced rotavirus vaccines have strict age recommendations for administration in accordance with the age when vaccine was administered in the clinical trials.8,9 In the 2006 recommendation for the routine use of RV5, ACIP recommended that the vaccine be administered at 2, 4, and 6 months of age with a minimum age of 6 weeks and maximum age of 12 weeks for the first dose. Subsequent doses were recommended at 4- to 10-week intervals so that all 3 doses are administered by 32 weeks of age.8 In 2008, when RV1 was added to the recommendation, the age limits were harmonized to accommodate the different dosing schedules for the 2 vaccines. The first dose of either rotavirus vaccine is now recommended between 6 weeks and 14 weeks and 6 days, with subsequent doses administered on at least 4 week intervals and all doses administered by 8 months and 0 days.9 Given the complexity of age at administration guidelines, assessing provider knowledge and compliance is important.

In a survey of pediatricians and family practice physicians in the fall of 2007, 69% of pediatricians and 30% of family practice providers knew the age by which the first dose of RV5 should be administered and 62% and 32%, respectively, knew the age by which all 3 doses should be administered.12 In practice, 12% of pediatricians and 20% of family practice providers reported that they frequently or sometimes gave the first dose of RV5 to infants >12 months of age, and 7% of pediatricians and 10% family practice providers reported frequently or sometimes administering the third dose to infants >32 weeks of age.12 Both pediatricians and family practice providers reported that the age recommendations were complex.

Available data suggest that the majority of US children vaccinated with RV5 have received their doses within the ACIP-recommended age windows. However, some children have been vaccinated outside these age windows. In a study using data from a large insurance claims database, 51% of children received their first dose of RV5 outside the recommended age window during the first 3 months of the RV5 vaccination program, although few children were vaccinated.16 During the first 6 months of the RV5 vaccination program, 20% of children selected by the Philadelphia immunization information system (IIS) received their first dose outside the recommended window.17 However, in assessments of vaccination data from sentinel IIS sites, the Vaccine Safety Datalink, and an insurance claims database though mid-2007, this proportion decreased to 7% to 14% (Fig. 1). 16,18 In all of these studies, only 2% to 4% of fully vaccinated children received the third dose of RV5 beyond the recommended upper age limit.16–18 No studies have yet examined the adherence to the updated age recommendations following the addition of RV1 to the immunization schedule.

Figure 1
Figure 1
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VACCINE UPTAKE AND COVERAGE

Nationally representative data on childhood vaccine coverage in the United States are provided by the National Immunization Survey. However, since the National Immunization Survey targets children 19 to 35 months of age, data on uptake of new vaccines recommended for use in infancy are not available in the early period postvaccine introduction. Estimates of rotavirus vaccine coverage are available from other data sources. Although these sources are not necessarily nationally representative, the consistency of the pattern of these sources is reassuring regarding the generalizability of the data.

One source that provides timely data on vaccine coverage is IISs.19 IISs are electronic immunization registries that are locally administered throughout the United States and collect and consolidate immunization records from multiple vaccination providers and administrative databases for children living in a defined catchment area. A subset of sentinel IIS sites with high healthcare provider participation (>85%), high child enrollment (>85% of children <19 years of age), and timely capture of administered vaccines (>70% of doses are reported to the IIS within 30 days of vaccine receipt) has been used to estimate rotavirus vaccine coverage in the United States.19 Although not nationally representative, the population-based IIS sentinel sites currently cover more than 1.8 million children <6 years of age residing in diverse regions throughout the United States (Arizona, Colorado, Michigan, Minnesota, New York City, North Dakota, Oregon, and Wisconsin).19

By June 30, 2009, ≥1 dose coverage with rotavirus vaccine among infants aged 5 months had reached a mean of 72% at the 8 sentinel IIS sites (range, 48%–86%).19 At 4 sentinel sites that provided data continuously since rotavirus vaccine was introduced in 2006 (Arizona, Michigan, Minnesota, and Oregon), ≥1 dose coverage with rotavirus vaccine among infants 5 months of age increased rapidly to 50% to 60% during the first year after introduction of vaccine and then increased steadily (2.7% per quarter on average) thereafter to 74% by the end of the second quarter of 2009 (Fig. 2). 19 However, 3 years after US licensure, rotavirus vaccine coverage still remained approximately 10 percentage points below the coverage levels of 2 other routine infant immunizations: Diphtheria-Tetanus-acellular Pertussis (DTaP) vaccine and pneumococcal vaccine.

Figure 2
Figure 2
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VACCINE EFFECTIVENESS

Prelicensure clinical trials in developed countries showed high efficacy for both the RV5 and RV1 vaccines that are currently available in the United States. In clinical trials in the United States and Europe, RV5 reduced hospitalizations due to rotavirus gastroenteritis by 96% (95% confidence interval [CI], 91%–98%), ED visits by 94% (95% CI, 89%–97%), and office visits by 86% (95% CI, 74%–93%).20 RV1 was 85% (95% CI, 71%–93%) efficacious in preventing severe (Vesikari score ≥11) rotavirus gastroenteritis during the first year of life in clinical trials in Latin America and 96% (95% CI, 90%–99%) efficacious against severe disease in Europe.21,22 Despite these promising efficacy data, the effectiveness of vaccine during routine use can differ from the efficacy observed during the ideal conditions of the clinical trial. Therefore, monitoring effectiveness postvaccine introduction is important.

To assess the effectiveness of rotavirus vaccination during routine use in the United States, rotavirus surveillance commenced in 2006. A case-control study of vaccine effectiveness was conducted using active surveillance at a large pediatric hospital in Houston, Texas in 2008, which enrolled children presenting with acute respiratory illness and children with rotavirus-negative acute gastroenteritis as controls. In this study, 3 doses of RV5 were 85% (95% CI: 55%–95%) and 89% (95% CI: 70%–96%) effective, respectively for the 2 different control groups, in preventing severe rotavirus gastroenteritis resulting in hospitalization or ED care and 100% (95% CI: 71%–100%) effective in preventing hospitalization due to rotavirus gastroenteritis.23 A partial series also provided substantial protection with 1 and 2 doses being 69% (95% CI: 13%–89%) and 81% (95% CI: 13%–96%) effective, respectively, against severe rotavirus gastroenteritis resulting in hospitalization or ED care for the 2 control groups combined. However, as most infants who began vaccination went on to receive the full series, these partial series estimates are largely based on relatively short 1 to 3 month periods of follow-up between vaccine doses.

In a study using an insurance claims database, 3 doses of RV5 were 100% (95% CI: 87%–100%) effective against rotavirus-coded hospitalizations and ED visits and 59% (95% CI: 47%-68%) effective against all-cause acute gastroenteritis requiring hospital or ED care.24 In the outpatient setting, 3 doses of RV5 were 96% (95% CI: 76%–100%) and 28% (95% CI: 22%–33%) effective against rotavirus-coded gastroenteritis and all-cause acute gastroenteritis, respectively.24 RV1-specific estimates of vaccine effectiveness are not yet available.

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VACCINE IMPACT

The introduction of rotavirus vaccine in the United States has had an immediate and dramatic impact on the epidemiology and burden of disease.25–28 Using data from the National Respiratory and Enteric Virus Surveillance System, a national, passive surveillance network of sentinel clinical laboratories that report weekly numbers of rotavirus tests performed and the number of positive results, trends in rotavirus testing and detection were analyzed. The timing and magnitude of the first 2 rotavirus seasons following vaccine introduction (2007–2008 and 2008–2009) were delayed by 15 and 6 weeks, respectively, and the peak proportion of positive tests decreased by 60% and 42%, respectively.25–27 Although the number of tests and the proportion positive for both postvaccine introduction seasons remained substantially below the prevaccine baseline, rotavirus activity appeared elevated and less delayed in the 2008–2009 rotavirus season compared with the 2007–2008 rotavirus season. Although some of the increased activity in the 2008–2009 season may be due to natural secular variation, part of the increased activity may also be due to an accumulation of susceptible children following the 2007–2008 season among whom rotavirus transmission was markedly decreased.29

In an analysis of discharge data from all hospitals located in 18 states representing 49% of the US population, rates of all-cause diarrhea hospitalizations among children <5 years of age during the rotavirus season declined 16% in 2007 and 46% in 2008 from a median of 101.1 per 10,000 during 2000–2006 to 85.5 per 10,000 in 2007 and 55.5 per 10,000 in 2008.28 (Fig. 3). This reduction was observed in all age groups. During the 2008 rotavirus season, an estimated 55,000 all-cause diarrhea hospitalizations in children <5 years were prevented, which corresponds to the elimination of 1 in every 20 hospitalizations among US children <5 years of age.28 A delayed peak in 2008 was also observed in hospital discharges for all-cause diarrhea among children <5 years of age.28 All-cause diarrhea hospital discharges peaked in February or March for children <5 years of age during the prevaccine years from 2000 to 2006. In 2008, a bimodal peak was observed with the second larger peak in April likely due to rotavirus.

Figure 3
Figure 3
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The peak rate of all-cause diarrhea hospitalizations in April 2008 was 64.5 per 10,000 children <5 years of age, which was one-half to two-thirds lower than the peak rates during 2000–2006.28 Declines in disease were seen in all children <5 years of age and not solely in vaccine-eligible children suggesting possible indirect protection among unvaccinated populations who were still at risk. Similarly, declines in disease among young children age-eligible to have received vaccine exceeded estimated vaccination coverage suggesting that unvaccinated age-eligible children were also indirectly benefitting from the rotavirus vaccination program. Rates of all-cause diarrhea hospitalization in 2008 decreased by 50% in children 6 to 23 months of age and by 30% to 45% among younger and older children compared with the 2000–2006 median rates during the rotavirus season.28

Surveillance among patients at a large pediatric practice in New Orleans also found significant declines in rotavirus and all-cause gastroenteritis healthcare visits among all children <5 years of age but was most pronounced among children age-eligible to have received vaccine.30 Compared with a 2004–2005 baseline, rotavirus-associated ED visits and hospitalizations decreased by 67% in 2007–2009. The decrease was greatest among children <2 years of age (81%). A smaller decrease of 41% was observed among children 2 years to <5 years of age. All-cause gastroenteritis office visits and hospitalizations decreased by 23% and 50%, respectively, in 2007–2009 compared with the 2004–2005 baseline. Vaccine coverage with ≥1 dose of RV5 increased from 11% in 2006–2007 to 40% in 2007–2008 and 46% in 2008–2009.

In another study using data from medical claims databases, large reductions in gastroenteritis visits were observed during the 2007–2008 rotavirus season compared with the baseline rotavirus seasons from 2003 to 2006 in inpatient, noninpatient, and physician office settings. Declines in gastroenteritis were seen in all age groups <5 years of age and were greater than the estimated vaccine coverage suggesting substantial indirect benefits of vaccine. Mean reductions in total gastroenteritis hospitalizations for children in the South, Midwest, and Northeast during the 2007–2008 rotavirus season compared with a 2003–2006 prevaccine baseline were 69% for children <1 year of age, 74% for children 1 year of age, 70% for children 2 years of age, and 67% for children 3 to 4 years of age; estimated coverage with ≥1 dose of rotavirus vaccine at the start of the 2007–2008 season ranged from 0% in children 2 to 4 years of age to 58% in children <1 year of age.31 Even larger declines were observed in gastroenteritis hospitalizations estimated to be due to rotavirus (those during the rotavirus season above the nonrotavirus season baseline): 96% for children <1 year of age, 89% for children 1 year of age, 85% for children 2 years of age, and 86% for children 3 to 4 years of age. Declines of ≥50% were also seen for total gastroenteritis visits in the noninpatient (including ED) and office settings during the rotavirus season among children <5 years of age.31 Overall, disease reductions in the West were lower than in the other regions.

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SUMMARY

Since its introduction into the national immunization program in 2006, the use of rotavirus vaccine has increased steadily in the United States although it still has lower coverage than other infant immunizations. Rotavirus vaccine has been widely accepted by pediatricians but acceptance by family practitioners initially lagged. In postlicensure evaluations, routine use of RV5 has been shown to be effective in preventing rotavirus diarrhea and vaccine use has resulted in substantial impact and changes in the epidemiology of rotavirus gastroenteritis in the United States. Rotavirus seasons have been delayed and diminished in magnitude during the postvaccine introduction era compared with the prevaccine era. Hospitalizations, ED visits, and outpatient visits for gastroenteritis have dramatically declined. These observed changes in the rotavirus season are consistent with models estimating the impact of vaccine introduction in the United States.29,32 However, the marked indirect benefits in age-ineligible and unvaccinated children were not anticipated and have greatly enhanced the impact of vaccination in the first years of the program.

RV1 was introduced in 2008 and little information is currently available about the effectiveness of RV1 in the US population. However, as use of this vaccine continues, calculation of RV1-specific vaccine effectiveness estimates should be possible. In March 2010, the use of RV1 was temporarily suspended in the United States by the Food and Drug Administration (FDA) after DNA from porcine circovirus (PCV) type 1 was found in commercial vials of RV1 by independent researchers using novel detection techniques.33 DNA fragments from PCV1 and the related PCV2 were also subsequently found in RV5.33 After a review of data regarding the finding of PCV and PCV DNA in rotavirus vaccines by FDA's Vaccine and Related Biologicals Product Advisory Committee, FDA determined that the demonstrated benefits of rotavirus vaccines outweighed the theoretical risks of PCV and recommended that providers resume the use of RV1 and continue the use of RV5.33 The impact of these findings and recommendations on vaccine coverage and acceptance is being monitored.

Continued monitoring of rotavirus seasons will enable assessment of whether immunity wanes as the vaccinated child ages. Further study is also needed to better quantify the indirect benefits of vaccination particularly changes in disease burden over time among age-ineligible and unvaccinated children. Finally, ongoing surveillance is needed to monitor in the long-term impact on rotavirus epidemiology and to assess vaccine impact on the circulating rotavirus strains, particularly whether population immunity could eventually result in selection of rotavirus strains against which vaccines are less protective. Although no evidence to date suggests that this has occurred, strain surveillance is needed to monitor for this possibility.

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REFERENCES

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Keywords:

rotavirus; rotavirus vaccine; vaccine impact

© 2011 Lippincott Williams & Wilkins, Inc.

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