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Pediatric Infectious Disease Journal:
doi: 10.1097/INF.0b013e3181ffe3eb
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Sustained Decline in Rotavirus Detections in the United States Following the Introduction of Rotavirus Vaccine in 2006

Tate, Jacqueline E. PhD; Mutuc, Jeffry D. MPH; Panozzo, Catherine A. MPH; Payne, Daniel C. PhD; Cortese, Margaret M. MD; Cortes, Jennifer E. MD; Yen, Catherine MD, MPH; Esposito, Douglas H. MD; Lopman, Benjamin A. PhD; Patel, Manish M. MSc, MD; Parashar, Umesh D. MB BS, MPH

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

Accepted for publication October 4, 2010.

The findings and conclusions of 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, 1600 Clifton Rd, NE, MS-A47, Atlanta, GA 30333. E-mail: jqt8@cdc.gov.

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Abstract

Background: Following implementation of the rotavirus vaccination program in 2006, rotavirus activity in the United States declined dramatically in 2007–2008 but increased slightly in 2008–2009, despite greater vaccine uptake. To further evaluate impact of the vaccine program, we assessed trends in rotavirus testing and detection during 2009–2010.

Methods: We examined rotavirus testing data from July 2000 to June 2010 from the National Respiratory and Enteric Viruses Surveillance System to compare rotavirus season timing and peak activity in the pre- and postvaccine introduction eras. Rotavirus season onset was defined as the first of 2 consecutive weeks during which the percentage of specimens testing positive for rotavirus was ≥10%. To assess trends in rotavirus testing and detection, we restricted the analyses to 25 laboratories that reported for ≥26 weeks per season from 2000 to 2010.

Results: During 2009–2010, the threshold for the start of the rotavirus season was never achieved nationally or in the North, Midwest, or West. Activity in the South met this threshold but the season duration was substantially shorter and of lower magnitude than in all previous pre- and postvaccine introduction seasons. Nationally and within each region, the peak week was more delayed and the peak proportion of positive tests was substantially lower than all previous seasons. The total number of tests performed declined by 23%, and the number of positive tests declined by 86%.

Conclusions: Rotavirus activity was substantially diminished during the 2009–2010 rotavirus season compared with the prevaccine baseline and the 2 previous postvaccine introduction seasons. These sustained declines over 3 rotavirus seasons reaffirm the health benefits of the US rotavirus vaccination program.

Following the introduction of pentavalent rotavirus vaccine in vaccination program in the United States in 2006, rotavirus activity changed dramatically. Laboratory surveillance data from the National Respiratory and Enteric Virus Surveillance System (NREVSS) showed that the rotavirus seasons in 2007–2008 and 2008–2009 were delayed in onset by 15 weeks and 6 weeks, respectively, and diminished in magnitude by 60% and 42%, respectively, compared with prevaccine years from 2000 to 2006.1,2 Although rotavirus activity was delayed and diminished during both seasons, the 2008–2009 rotavirus season, despite greater vaccine uptake, unexpectedly began earlier and was modestly elevated compared with the 2007–2008 season. In this report, we examined NREVSS data for the recently concluded 2009–2010 rotavirus season to further assess national and regional trends in rotavirus testing and detection in the United States.

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METHODS

As a passive, national network of collaborating university and community hospital laboratories, selected state and county public health laboratories, and commercial laboratories in the United States, NREVSS monitors temporal and geographic trends for various viral pathogens, including rotavirus.3 Each week, participating laboratories report to the Centers for Disease Control and Prevention aggregate data on the number of rotavirus antigen detection tests performed and the number of positive results obtained using commercially available enzyme immunoassays. No clinical and epidemiological data are reported.

We examined data from July 2000 through June 2010. Year-long seasons were defined as July through June of the following year. We compared data aggregated by week from the 2009–2010 season with 6 prevaccine seasons from July 2000 through June 2006 and 2 postvaccine introduction seasons from July 2007 through June 2008 and July 2008 through June 2009, as reported earlier.1,2 We excluded data from the July 2006 through June 2007 season because it was a transitional year for vaccine introduction, and uptake was likely unevenly distributed within regions. Approximately 66 laboratories (range, 61–72) contributed data to NREVSS each season between July 2000 and June 2010.

Data from all laboratories that reported during a given calendar week were used to compare the timing of the pre- and postvaccine introduction seasons nationally and regionally for each of the following 4 US census regions: West, South, Midwest, and North. In NREVSS, the rotavirus season onset has been defined as the first of 2 consecutive weeks during which the percentage of specimens testing positive for rotavirus was ≥10%.1,2 The peak of the rotavirus season was the week with the highest proportion of rotavirus positive tests. The end of the rotavirus season was defined as the last of 2 consecutive weeks during which the percentage of specimens testing positive for rotavirus was ≥10%.

To characterize national and regional trends in rotavirus testing and detection, we examined a subset of 25 NREVSS laboratories that consistently reported for ≥26 weeks per season for 10 consecutive seasons from July 2000 through June 2010. The total number of tests, the total number of positive tests, and the proportion of positive tests for the July 2009 through June 2010 season were compared with the median values for each of these parameters for the 6 prevaccine seasons from July 2000 through June 2006 and for the first 2 postvaccine introduction seasons of July 2007 through June 2008 and July 2008 through June 2009. To smooth the curves for the number of tests performed and the number of positive specimens detected, we used a 3-week unweighted moving average for the national data and for data from the West, South, and Midwest. A 5-week unweighted moving average for data from the North was used due to the small number of participating laboratories.

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RESULTS

Nationally, during the 2009–2010 season, no 2 consecutive surveillance weeks had a proportion of rotavirus positive tests that were ≥10% (Fig. 1A). Thus, the criteria for the start and end of the rotavirus season were not met. Rotavirus activity peaked during May (week 18) with 11% of tests positive for rotavirus. Only 2 other weeks during this season had a proportion of positive tests ≥10% (week 16, 10% positivity and week 20, 11% positivity). By region, the criteria for the start and end of the rotavirus season were not met in the North, Midwest, and West (Fig. 1B, D, E). The proportion of rotavirus tests peaked in May in the North (week 20, 13% positivity) and in the West (week 18, 12% positivity). In the Midwest, a peak of 13% occurred in October (week 43) and a second peak of 12% occurred in May (week 19). The criteria for the start and end of the rotavirus season were met in the South, with the season beginning in April (week 15) and ending in June (week 24) (Fig. 1C). However, in 3 nonconsecutive weeks of the 10 weeks during this season, the proportion of rotavirus positive tests was <10%. Rotavirus activity peaked in the South in May (week 18) with 18% of tests positive for rotavirus.

Figure 1
Figure 1
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From July 2000 through June 2010, 25 NREVSS laboratories consistently reported rotavirus test results for ≥26 weeks during each season including 9 laboratories located in the South, 8 in the West, 6 in the Midwest, and 2 in the North. The total number of tests performed decreased 23% from a median of 12,828 tests during the prevaccine era to 9909 tests in 2009–2010, and the number of positive tests decreased 86% from a median of 3279 positive tests during the prevaccine era to 451 positive tests in 2009–2010. A corresponding decrease of 82% was observed in the rotavirus detection rate from a median of 26% in the prevaccine era to 5% during the 2009–2010 season. During the 2009–2010 season, the total number of rotavirus tests, the number of positive rotavirus tests, and the rotavirus detection rate were all lower than the figures during each of the 2007–2008 and 2008–2009 postvaccine seasons (Table 1, Fig. 2A).

Table 1
Table 1
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Figure 2
Figure 2
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Similar trends in rotavirus testing and detection were seen in each of the 4 regions (Table 1). The number of tests performed during the 2009–2010 season in every region was below the 2000–2006 prevaccine baseline ranging from a 9% decrease in the West to a 41% decrease in the North. In each of the regions, the number of positive rotavirus tests in 2009–2010 was 83% to 93% lower than the prevaccine baseline. The rotavirus detection rate during 2009–2010 was 8% in the North, 7% in the South, 4% in the West, and 3% in the Midwest representing a 72%, 74%, 81%, and 91% decrease in the rotavirus detection rate from the prevaccine baselines, respectively. Of the 3 postvaccine seasons, the 2009–2010 season had the greatest decrease in the number of total rotavirus tests performed, the number of positive rotavirus tests, and the proportion positive compared with the prevaccine baselines in all regions (Table 1, Fig. 2B–E).

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DISCUSSION

The dramatic changes in rotavirus activity observed during the first 2 rotavirus seasons following the vaccine introduction in the United States were sustained and enhanced during the most recent 2009–2010 season. Rather than just a delay in the start and a reduction in the duration of the season as was observed in the 2007–2008 and 2008–2009 seasons, the reduction in rotavirus activity in 2009–2010 was so pronounced that the a priori threshold of 2 consecutive weeks with ≥10% positive tests that defines the start of the epidemic rotavirus season was never achieved nationally or in the North, Midwest, or West. Activity in the South met this threshold, but the season duration of 10 weeks was substantially shorter than the prevaccine baseline of 25 weeks and of the 2 postvaccine introduction seasons of 13 and 23 weeks in 2007–2008 and 2008–2009, respectively. Nationally and in all regions, the peak week was more delayed and the peak proportion of positive tests was substantially lower in the 2009–2010 season compared with the prevaccine baseline and the first 2 postvaccine introduction seasons. Additionally, for the first time since vaccine introduction, the total number of rotavirus tests performed decreased compared with the prevaccine baseline. The proportional decline in rotavirus positive tests (86%) was far greater than the decline in the total tests performed (23%), suggesting that the decline in healthcare visits related to rotavirus was driving the decrease in the number of tests performed after vaccination.

The sustained declines in rotavirus activity during 3 postvaccine seasons reaffirm that these changes are attributed to the rotavirus vaccination program. Rotavirus vaccine coverage has risen steadily since its introduction in 2006. At 4 sentinel immunization information sites that have provided data continuously since 2006, ≥1 dose coverage with rotavirus vaccine among infants 5 months of age increased rapidly to 50% to 60% during the first year postvaccine introduction and increased steadily thereafter to 72% by the end of the second quarter of 2009.4 For the 2007–2008 season, the reductions seen with NREVSS data are supported by several reports documenting a decline in health care utilization for diarrhea and rotavirus in US children.5–7 These reports also documented substantial declines in children >2 years of age who were age ineligible for vaccination, suggesting indirect benefits (ie, herd immunity) from vaccination.6,7 Similar to that observed in the NREVSS data, an analysis of hospital discharge data from a national sample of hospitals showed an increase in rotavirus activity during the 2008–2009 season compared with 2007–2008, and in the hospital discharge data, most of this increase occurred in children >2 years of age.8 It is possible that, given the marked decline in rotavirus activity during 2007–2008, more older, unvaccinated, susceptible children had accumulated during 2008–2009 season who had not been exposed to rotavirus in the previous season, resulting in greater activity during 2008–2009. In 2009–2010, continued increases in vaccination coverage coupled with a depletion of rotavirus susceptible children during the previous season may have resulted in the extremely diminished rotavirus activity. These short-term dynamics are predicted by mathematical models of rotavirus transmission and not an indication of vaccine failure or reduced uptake.9,10 While some similar secular variation is likely in future years, increasing immunization coverage among progressively older age groups should keep rotavirus activity at low levels.

Data from NREVSS have several limitations. First, due to aggregate data reporting, no information on patient demographics or clinical characteristics are collected, which precludes analyses by age or vaccination status. Further, because no patient level data are available, a given patient might have multiple test results reported in NREVSS. Second, while participating laboratories are located in all regions of the country, data from NREVSS may not reflect national or regional trends in rotavirus testing and detection. Finally, reporting to NREVSS is voluntary and testing for rotavirus is not part of standard clinical practice. Rotavirus testing was performed at the discretion of the physician and based on institutional practices. Changes in such practices over time may have some influence on our findings, but these changes are unlikely to explain the consistent and large declines observed in the 3 postvaccine seasons. Furthermore, consistency in the declines for both the 2007–2008 and 2008–2009 seasons with other studies is reassuring.6,7,11

In conclusion, rotavirus activity was substantially diminished during the 2009–2010 rotavirus seasons compared with the prevaccine baseline and the 2 previous postvaccine introduction seasons. These changes occurred concomitantly with increased rotavirus vaccination coverage and may have been further influenced by indirect protective benefits of the vaccine on unvaccinated young children. Further study of the 2009–2010 season, including active surveillance for rotavirus confirmed cases and examination of hospital discharge data, will help confirm and refine our findings.

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REFERENCES

1.Tate JE, Panozzo CA, Payne DC, et al. Decline and change in seasonality of US rotavirus activity after the introduction of rotavirus vaccine. Pediatrics. 2009;124:465–471.

2.Centers for Disease Control and Prevention. Reduction in rotavirus after vaccine introduction—United States, 2000–2009. Morb Mortal Wkly Rep. 2009;58:1146–1149.

3.Centers for Disease Control and Prevention. National Respiratory and Enteric Virus Surveillance System. Available at: http://www.cdc.gov/surveillance/nrevss/rotavirus/default.html. Accessed 18 September, 2010.

4.Centers for Disease Control and Prevention. Rotavirus vaccination coverage among infants aged 5 months—immunization information system sentinel sites, United States, June 2006–June 2009. Morb Mortal Wkly Rep. 2010;59:521–524.

5.Begue RE, Perrin K. Reduction in gastroenteritis with the use of pentavalent rotavirus vaccine in a primary practice. Pediatrics. 2010;126:e40–e45.

6.Cortese MM, Tate JE, Simonsen L, et al. Reduction in gastroenteritis in United States children and correlation with early rotavirus vaccine uptake from national medical claims databases. Pediatr Infect Dis J. 2010;29:489–494.

7.Curns AT, Coffin F, Glasser JW, et al. Projected impact of the new rotavirus vaccination program on hospitalizations for gastroenteritis and rotavirus disease among US children <5 years of age during 2006–2015. J Infect Dis. 2009;200(suppl 1):S49–S56.

8.Yen C, Tate JE, Wenk JD, et al. Diarrhea-associated hospitalizations among US children over two rotavirus seasons after vaccine introduction. Pediatrics. In Press.

9.Pitzer VE, Viboud C, Simonsen L, et al. Demographic variability, vaccination, and the spatiotemporal dynamics of rotavirus epidemics. Science. 2009;325:290–294.

10.Atchison C, Lopman B, Edmunds WJ. Modelling the seasonality of rotavirus disease and the impact of vaccination in England and Wales. Vaccine. 2010;28:3118–3126.

11.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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Keywords:

rotavirus; surveillance; vaccine impact

© 2011 Lippincott Williams & Wilkins, Inc.

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