PEDIATRICS Vol. 115 No. 6 June 2005, pp. 1488-1493 (doi:10.1542/peds.2004-1826)
Vaccine Effectiveness During a Varicella Outbreak Among Schoolchildren: Utah, 2002–2003
,
* Epidemic Intelligence Service, Epidemiology Program Office
¶ Viral Vaccine-Preventable Diseases Branch, Epidemiology and Surveillance Division, National Immunization Program
** Division of Applied Public Health Training, Epidemiology Program Office
National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
Utah Department of Health, Salt Lake City, Utah
Salt Lake Valley Health Department, Salt Lake City, Utah
|| University of Utah School of Medicine and Primary Children’s Medical Center, Salt Lake City, Utah
 |
ABSTRACT |
|---|
 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Objectives. In the context of a chickenpox outbreak involving 2 Utah elementary schools, we conducted an investigation to assess vaccine effectiveness, describe illness severity, and examine risk factors for breakthrough varicella (ie, varicella in those who have been vaccinated).
Methods. All parents were asked to complete a questionnaire about their child’s medical history. Parents of children with recent varicella were interviewed, and vaccination records were verified. Lesions were submitted for polymerase chain reaction testing.
Results. Questionnaires were returned for 558 (93%) of 597 students in school A and 924 (97%) of 952 students in school B. A total of 83 schoolchildren (57 unvaccinated and 26 vaccinated) had varicella during the October 2002 through February 2003 outbreak period. An additional 17 cases occurred among household contacts, including infants and adults. Polymerase chain reaction analysis recovered wild-type varicella. Vaccine effectiveness was 87%. With 1 notable exception, vaccinated children tended to have milder illness. Risk factors for breakthrough varicella included eczema, vaccination 
5 years before the outbreak, and vaccination at 
18 months of age. Restricting analysis to children vaccinated 5 years before the outbreak, those vaccinated at 18 months of age were more likely to develop breakthrough varicella (relative risk: 9.3; 95% confidence interval: 1.3–68.9).
Conclusions. The vaccine, administered by >100 health care providers to 571 children during a 7-year time period, was effective. Risk factors for breakthrough varicella suggest some degree of biological interaction between age at vaccination and time since vaccination.
Key Words: pediatrics • school-age population • vaccination • varicella-zoster virus
Abbreviations: PCR, polymerase chain reaction • ARU, attack rates among the unvaccinated • ARV, attack rates among the vaccinated • RR, relative risk • CI, 95% confidence interval
Although primary infection with varicella zoster virus is usually benign, varicella caused 
11000 hospitalizations and 100 deaths annually in the United States before licensure of a vaccine in 1995. Most deaths and hospitalizations occurred in previously healthy persons without underlying immunocompromising conditions.1,2 After vaccine licensure, as vaccine coverage among children increased, varicella incidence decreased across all age groups.3
Despite these declines, chickenpox outbreaks continue to occur, including outbreaks in vaccinated populations.4–7 Outbreaks might generate concerns that vaccine effectiveness is lower under real-life conditions than the 70% to 90% predicted by prelicensure studies.8 Indeed, vaccine effectiveness was only 44% during a 2000–2001 outbreak in a New Hampshire day care5 and 56% during a 2002 outbreak in a Minnesota elementary school.7
The Advisory Committee on Immunization Practices recommends varicella vaccination for all children aged 12 to 18 months and advises that vaccination or other evidence of immunity be required for school entry.8,9 Utah implemented a new vaccination requirement for kindergarten children in 2002. The vaccination requirement will increase by 1 grade each year, following that cohort forward in time, so that by 2014 no child may enter kindergarten through grade 12 without evidence of varicella immunity. Exemptions are available for children with medical contraindications or whose parents have personal or religious beliefs against vaccination.
During the 2002–2003 school year, a varicella outbreak was detected after a vaccinated child developed varicella complicated by severe group A streptococcal cellulitis requiring hospitalization. The child’s parents observed that other vaccinated classmates at the child’s elementary school also had varicella. School nurses corroborated this observation, reporting numerous chickenpox cases at 2 elementary schools in the same school district, and also that many parents, school staff, and community health care providers were voicing concerns about the effectiveness of the vaccine. We conducted an investigation to assess vaccine effectiveness, describe illness severity, and examine risk factors for breakthrough varicella.
|
METHODS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
All students at both schools took home a letter explaining the study and requesting parents’ (or guardians’) voluntary participation. Each school served children in kindergarten through grade 6 (ages 5–12 years), with 24 classes in school A (597 students) and 37 classes in school B (952 students) during the 2002–2003 school year. Parents completed a questionnaire about their child’s classroom, gender, birth date, varicella history, varicella vaccination date and provider, medications, and history of conditions including asthma and eczema; they also provided consent to verify their children’s vaccination history.
When a returned questionnaire reported recent varicella-like illness, we interviewed parents to elicit more details about the illness severity. A varicella case was defined as rash illness without other apparent cause. Varicella classically presents with an acute onset of a pruritic maculopapulovesicular rash. Breakthrough varicella might not progress to the vesicular stage,10 so parental classification of varicella was accepted for some vaccinated children with mild cases who had epidemiologic links to persons with classic cases. Rashes of <50 lesions were classified as mild, 50 to 500 as moderate, and >500 as severe; illness was also classified as severe if associated with fever lasting 5 days, invasive complications, or hospitalization. Illness that occurred >42 days after vaccination was considered breakthrough.
Individual vaccination status was verified by the Utah Statewide Immunization Information System and vaccination records. Vaccine records were systematically obtained for children in any of the following categories: (1) a child with varicella during the 2002–2003 school year regardless of reported vaccination status; (2) a reportedly unvaccinated child with no history of varicella and no varicella during the school year; (3) a reportedly vaccinated child; or (4) a student in kindergarten through grade 3. Because of resource constraints, records were not obtained for reportedly unvaccinated older children with a prior history of varicella.
Parents of children with existing rash were asked to allow sampling of lesions for polymerase chain reaction (PCR) testing at the Centers for Disease Control and Prevention National Varicella Laboratory. Virus was amplified by use of consensus varicella zoster primers as previously described.11 PCR products were sequenced and compared with known vaccine and wild-type sequences.
All children for whom parents remembered a primary varicella episode before October 1, 2002, were excluded from calculation of the attack rates used to determine vaccine effectiveness. We calculated attack rates among the unvaccinated (ARU) as the number of varicella cases among the unvaccinated divided by the total number of unvaccinated children without a history of varicella. Attack rates among the vaccinated (ARV) were the number of breakthrough cases divided by the total number of vaccinated children. Vaccine effectiveness was calculated as (ARU – ARV)/ARU x 100.12,13 We calculated a separate attack rate to measure the incidence of an outbreak-associated second occurrence of varicella among unvaccinated children with a prior history of varicella.
Unvaccinated children with a second occurrence of varicella were excluded from comparisons of illness severity. Differences in disease characteristics between vaccinated and unvaccinated children were examined by using Fisher’s exact test for dichotomous variables, the Wilcoxon-Mann-Whitney test for ordered categories,14 and the Wilcoxon rank-sum statistic for continuous variables.
We calculated the relative risk (RR), given different risk factors, of breakthrough varicella. All P values and 95% confidence intervals (CIs) were 2-sided, with P values <.05 and CI excluding 1.0 considered significant. SAS 8.2 (SAS Institute, Cary, NC) and StatXact (Cytel, Cambridge, MA) software was used. For disease characteristics and risk factors for breakthrough varicella, no difference was found between the 2 schools, and the results were pooled.
As a public health response to an outbreak, this investigation was determined not to be human-subjects research.
|
RESULTS |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Questionnaires were returned for 558 (93%) of 597 students in school A and 924 (97%) of 952 students in school B. Based on parental recall, 91% of the children had presumptive immunity before the outbreak. Sources of varicella immunity, determined by history of infection or vaccination, were similar in the 2 schools. Children in grades 3 and higher were more likely to have had prior infection (grade-level range: 58–80%); younger children, born after vaccine licensure in 1995, were more likely to be vaccinated (range: 57–78%).
The outbreak began in October 2002 and continued until February 2003; 83 children met the case definition (Fig 1). The index case was in a susceptible unvaccinated first-grader with known exposure to varicella while visiting another part of the state in early October. In both schools, most cases occurred in grades 1 and 2. Every grade level except the school A kindergarten had cases. Some household transmission among enrolled siblings likely occurred; the 83 cases represented 66 households (relationships not shown). In addition, 17 secondary cases occurred among household contacts (age range: 1 month to 32 years) who did not attend either school, bringing the total number of known outbreak-related cases to 100.
|
Varicella vaccination could be verified for 432 (79%) of the 545 well children reported by parents to be vaccinated before the outbreak. For those whose vaccine receipt could not be verified (usually because of out-of-state vaccine administration), parents for 67 (13%) provided a precise vaccination date. For the remaining 46 (8%) well children, parental recall was the only evidence of vaccination. Questionnaire responses initially suggested that 38 children had breakthrough varicella. However, varicella-vaccine receipt could only be verified for 26 (68%) of those 38. Parents of the remaining 12 children were able to locate neither vaccination date nor provider name in their home records. During follow-up conversations, it was determined that these parents had mistakenly assumed that their children had received the varicella vaccine (ie, children who were up to date on all required vaccines but were too old for the new kindergarten requirement). Therefore, these 12 children were reclassified as unvaccinated. For the 481 vaccinated children whose provider was documented by either parents or records, administration locations included 25 pediatric and 20 family practice offices, 6 public health department clinics, 3 community health centers, 2 mobile vaccination clinics, and >50 out-of-state settings. No varicella-vaccination records could be found for any of the children reported by parents to be unvaccinated.
There were 48 primary cases in unvaccinated children and 26 breakthrough cases in vaccinated children attending the 2 schools during the outbreak period. In addition, parents of 9 unvaccinated children reported that their child’s outbreak-associated varicella was a second occurrence, with the prior episode occurring before October 1, 2002. PCR analysis detected varicella of the wild-type strain in specimens collected from 5 unvaccinated and 3 vaccinated children; specimens collected from an additional 2 vaccinated children were insufficient for testing.
In school A, there were 18 varicella cases among the 66 unvaccinated children without a history of varicella (ARU: 27%) and 8 among the 223 vaccinated children (ARV: 4%). In school B, there were 30 cases among the 74 unvaccinated children without a history of varicella (ARU: 41%) and 18 among the 348 vaccinated children (ARV: 5%). Vaccine effectiveness against varicella of any severity was 87% in each school (CI: 71–94% and 78–92%, respectively). Effectiveness against moderate or severe varicella was 90% (CI: 76–96%) for school A and 99% (CI: 94–99%) for school B. The estimates were similar (ie, effectiveness of 82% against any varicella) when analysis excluded the 113 reportedly vaccinated well students whose vaccine status could not be verified. Vaccine effectiveness was also similar after excluding the 8 children whose varicella onset date occurred after an enrolled sibling of the same household had developed varicella. Among unvaccinated children with a history of varicella, the varicella attack rate was 0.4% (1 of 269) in school A and 1.4% (8 of 502) in school B.
Compared with unvaccinated children with varicella, vaccinated children tended to have mild varicella (15% of unvaccinated vs 69% of vaccinated) of shorter duration (median days unable to play: 3 vs 1.5). However, parents were equally likely to consult health care providers (Table 1). One vaccinated child had severe varicella (39.7°C fever, >500 lesions) that required a 3-day hospitalization and intravenous antibiotics for management of group A streptococcal secondary skin infection; the child recovered fully.
|
Children with a history of eczema were 3.8 times more likely than those without eczema to develop breakthrough varicella (CI: 1.8–7.1). Both time since vaccination and age at vaccination differed between those vaccinated children who developed varicella and those who remained well. Compared with children vaccinated more recently, children vaccinated
5 years before the outbreak were more likely to develop breakthrough varicella (RR: 3.0; CI: 1.4–6.4). Compared with children vaccinated at an older age, those vaccinated at 18 months of age were more likely to develop breakthrough varicella (RR: 2.6; CI, 1.2–5.6) (Table 2). Restricting analysis to the 163 children vaccinated 5 years before the outbreak (ie, from March 30, 1995, through October 1, 1997), those vaccinated at 18 months of age were 9.3 times more likely than those vaccinated after 18 months old to develop breakthrough varicella (14 of 98 vs 1 of 65; CI: 1.3–68.9).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
This study supports the utility of the varicella-vaccination requirement for schoolchildren. The vaccine was highly effective, with estimated effectiveness in the upper range of that achieved by prelicensure trials, after administration outside controlled conditions by >100 health care providers to 571 children during a 7-year time period.
Despite the high vaccine effectiveness found by this study, one breakthrough case was severe enough to warrant hospitalization. Primary vaccine failure (ie, vaccine fails to stimulate a protective immune response when it is administered) is plausible for a small number of those who received the vaccine.10 The original perception of a high vaccine-failure rate in this population was influenced not only by some parents’ mistaken assumptions that their children were vaccinated but also by the high vaccine coverage, resulting in many cases, despite a low attack rate, among vaccinated children. Modeling predicts that varicella-vaccine coverage will need to reach 97% to achieve the background immunity required to prevent outbreaks,15 suggesting that outbreaks of varicella will continue to occur and that they will likely involve substantial numbers of vaccinated individuals.16
Children born after 1995 form a cohort more likely to acquire varicella immunity from vaccination. Widespread uptake of the varicella vaccine is associated with declining varicella incidence and circulation of the wild-type varicella virus. Health care providers should verify the vaccination status of older children who are not subject to a school-entry requirement and might remain susceptible during adulthood when varicella can be severe. Health care providers must not miss opportunities to offer vaccination to all eligible persons without a history of varicella. For example, a 32-year-old mother who developed a moderate case of primary varicella 15 days after her schoolchild developed mild breakthrough varicella was not aware that the vaccine given to her children was also available to adults without varicella immunity.
Breakthrough varicella has been associated previously with asthma.17,18 This study found no association between asthma and the risk of breakthrough varicella, but a history of eczema was associated with a higher risk of breakthrough varicella. Whether this association represents a real risk factor (eg, altered cell-mediated immunity),19 unrecognized confounding, or reporting bias is uncertain. This study relied on a parental questionnaire to document medical history, and parents of children with breakthrough varicella might have completed the questionnaire more attentively.
Our results confirm earlier reports that found time since vaccination5–7 and early age at vaccination4,18 to be risk factors for breakthrough varicella. A recent case-control study by Vazquez et al20 found vaccine effectiveness to be lower during the first year after vaccination for children vaccinated at <15 months of age. In the context of the varicella outbreak we studied, early age at vaccination remained a risk factor for breakthrough varicella within the subgroup of children vaccinated 5 years before, suggesting some degree of biological interaction between age at vaccination and time since vaccination. One hypothesis is that immunity wanes with time and the initial response to vaccination is attenuated when given at a younger age, leading to a greater impact from the subsequent passage of time. On the other hand, if waning immunity were a major risk factor, we might expect vaccine effectiveness to decline steadily with time, but the Vazquez study found vaccine effectiveness to be stable during the second through eighth years after vaccination.20
Our study is subject to several limitations, including bias and misclassification. In this outbreak, most cases occurred in grades 1 and 2 among children born soon after the vaccine became available and thus more likely to have a longer time since vaccination. However, time since vaccination might have also correlated with risk of varicella exposure, because the proportion of cases in the grade 1 and 2 classes implies that classmates had a greater risk of exposure during this outbreak. Parental reporting of varicella history was accepted as valid; serologic evidence of immunity or susceptibility was not sought. Of the 771 unvaccinated children presumed to have naturally acquired immunity based on parental recall of a varicella episode before October 1, 2002, at least 9 were still susceptible, because they developed an apparent second episode of varicella during the outbreak period. Because these 771 children were excluded from vaccine-effectiveness calculations, if a substantial number were actually susceptible, vaccine effectiveness in this outbreak would be lower than the calculated 87%. Conversely, some unvaccinated children thought to be still susceptible might have acquired immunity during an earlier illness that parents did not recognize as varicella. On the basis of the lower attack rates seen at the older grade levels, we suspect that the latter type of misclassification was more likely.
Several strengths distinguish this investigation. To our knowledge, this is the largest varicella outbreak to be studied systematically since the vaccine was licensed in the United States. We had adequate numbers to examine the joint effects of age at vaccination and time since vaccination. PCR analysis provided laboratory confirmation of wild-type varicella for a number of unvaccinated (n = 5) and vaccinated (n = 3) students. Excellent response rates contributed to completeness of case ascertainment. Verification of vaccine records helped minimize misclassification; otherwise, 12 unvaccinated children would have been misclassified as having breakthrough varicella, resulting in a much lower vaccine-effectiveness estimate.
Controlled, clinical trials cannot anticipate the complex interactions of the changing childhood immunization schedule, new school-entry requirements, and decreasing circulation of wild-type varicella virus. Continued data from outbreak and observational studies are needed to clarify the role of age at vaccination and the potential for waning immunity. If deferring vaccination until children are >18 months of age confers an improved immune response, that advantage might be offset by the risk of leaving younger children susceptible to primary infection. In addition, health care providers might be justifiably reluctant to miss any vaccination opportunities with 12-month-old children. As the epidemiology of varicella in the United States continues to evolve, our improved understanding of the long-term benefits and limitations of universal varicella vaccination will clarify whether adjustments to vaccination policies, such as adding a booster vaccine dose,21 are warranted.
|
ACKNOWLEDGMENTS |
|---|
This work was funded by the Utah Department of Health and Centers for Disease Control and Prevention.
The principals, staff, and families of schools A and B shared not only data but also invaluable enthusiasm for this investigation; we are particularly grateful to school nurses Sharee Merkley and Jody Stubler. Tim Duffy and pediatricians affiliated with Primary Children’s Medical Center first brought this outbreak to our attention. Dagmar Vitek, Sue Nicodemus, and Ilene Risk with the Salt Lake Valley Health Department and Linda Abel, Nicole Stone, and Phil Gresham with the Utah Department of Health facilitated study-related discussions with the school district, vaccine providers, and Utah’s Vaccine Advisory Committee. Nancy Pare and Sandra Schulthies expedited vaccine-record verifications through use of the Utah Statewide Immunization Information System. Xavier Cabezas and Susana Crane translated study instruments into Spanish. Vladimir Loparev and Scott Schmid (Centers for Disease Control and Prevention) provided specimen testing. Epidemic Intelligence Service officers Bhrett Lash, Mona Marin, and Barna Tugwell participated in early discussions about the study objectives and design. Lois Haggard (Utah Department of Health) advised the statistical analysis; C. Kay Smith-Akin (Centers for Disease Control and Prevention) gave editorial assistance; and Janet Blair (Centers for Disease Control and Prevention) contributed critical review of the manuscript.
|
FOOTNOTES |
|---|
Accepted Oct 4, 2004.
Address correspondence to Maryam B. Haddad, MSN, MPH, FNP, Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, Department of Health and Human Services, 1600 Clifton Rd, Mailstop E-10, Atlanta, GA 30333. E-mail: maryam.haddad{at}cdc.hhs.gov
This work was presented in part at the 41st Annual Meeting of the Infectious Diseases Society of America; October 9–12, 2003; San Diego, CA.
No conflict of interest declared.
|
REFERENCES |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
- Meyer PA, Seward JF, Jumaan AO, Wharton M. Varicella mortality: trends before vaccine licensure in the United States, 1970–1994. J Infect Dis. 2000;182 :383 –390[CrossRef][Web of Science][Medline]
- Galil K, Brown C, Lin F, Seward J. Hospitalizations for varicella in the United States, 1988 to 1999. Pediatr Infect Dis J. 2002;21 :931 –935[CrossRef][Web of Science][Medline]
- Seward JF, Watson BM, Peterson CL, et al. Varicella disease after introduction of varicella vaccine in the United States, 1995–2000.
JAMA. 2002;287
:606
–611
[Abstract/Free Full Text] - Galil K, Fair E, Mountcastle N, Britz P, Seward J. Younger age at vaccination may increase risk of varicella vaccine failure. J Infect Dis. 2002;186 :102 –105[CrossRef][Web of Science][Medline]
- Galil K, Lee B, Strine T, et al. Outbreak of varicella at a day-care center despite vaccination.
N Engl J Med. 2002;347
:1909
–1915
[Abstract/Free Full Text] - Tugwell BD, Lee LE, Gillette H, Lorber EM, Hedberg K, Cieslak PR. Chickenpox outbreak in a highly vaccinated school population.
Pediatrics. 2004;113
:455
–459
[Abstract/Free Full Text] - Lee BR, Feaver SL, Miller CA, Hedberg CW, Ehresmann KR. An elementary school outbreak of varicella attributed to vaccine failure: policy implications. J Infect Dis. 2004;190 :477 –483[CrossRef][Web of Science][Medline]
- Centers for Disease Control and Prevention. Prevention of varicella: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 1996;45 (RR-11):1–36
- Centers for Disease Control and Prevention. Prevention of varicella. Update recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 1999;48 (RR-6):1–5
- Centers for Disease Control and Prevention. Varicella (chickenpox) clinical case definition. Available at: www.cdc.gov/epo/dphsi/casedef/varicella_current.htm. Accessed April 5, 2004
- Loparev VN, Argaw T, Krause PR, Takayama M, Schmid DS. Improved identification and differentiation of varicella-zoster virus (VZV) wild-type strains and an attenuated varicella vaccine strain using a VZV open reading frame 62-based PCR.
J Clin Microbiol. 2000;38
:3156
–3160
[Abstract/Free Full Text] - Comstock GW. Evaluating vaccination effectiveness and vaccine efficacy by means of case-control studies.
Epidemiol Rev. 1994;16
:77
–89
[Free Full Text] - Orenstein WA, Bernier RH, Hinman AR. Assessing vaccine efficacy in the field.
Epidemiol Rev. 1988;10
:212
–241
[Free Full Text] - Moses LE, Emerson JD, Hosseini H. Analyzing data from ordered categories. N Engl J Med. 1984;311 :442 –448[Abstract]
- Halloran ME, Cochi SL, Lieu TA, Wharton M, Fehrs L. Theoretical epidemiologic and morbidity effects of routine varicella vaccination of preschool children in the United States.
Am J Epidemiol. 1994;140
:81
–104
[Abstract/Free Full Text] - Fine PEM, Zell ER. Outbreaks in highly vaccinated populations: implications for studies of vaccine performance.
Am J Epidemiol. 1994;139
:77
–90
[Abstract/Free Full Text] - Izurieta HS, Strebel PM, Blake PA. Postlicensure effectiveness of varicella vaccine during an outbreak in a child care center.
JAMA. 1997;278
:1495
–1499
[Abstract/Free Full Text] - Verstraeten T, Jumaan AO, Mullooly JP, et al. A retrospective cohort study of the association of varicella vaccine failure with asthma, steroid use, age at vaccination, and measles-mumps-rubella vaccination. Pediatrics. 2003;112 (2). Available at: www.pediatrics.org/cgi/content/full/112/2/e98
- Engler RJM, Kenner J, Leung DYM. Smallpox vaccination: risk considerations for patients with atopic dermatitis. J Allergy Clin Immunol. 2002;110 :357 –365[CrossRef][Web of Science][Medline]
- Vazquez M, LaRussa PS, Gershon AA, et al. Effectiveness over time of varicella vaccine.
JAMA. 2004;291
:851
–855
[Abstract/Free Full Text] - Gershon AA. Varicella vaccine—are two doses better than one [editorial]?
N Engl J Med. 2002;347
:1962
–1963
[Free Full Text]
PEDIATRICS (ISSN 1098-4275). ©2005 by the American Academy of Pediatrics
CiteULike 
Connotea 
Del.icio.us 
Digg 
Facebook 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  D. Perella, A. G. Fiks, A. Jumaan, D. Robinson, P. Gargiullo, J. Pletcher, C. M. Forke, D. S. Schmid, M. Renwick, F. Mankodi, et al. Validity of Reported Varicella History as a Marker for Varicella Zoster Virus Immunity Among Unvaccinated Children, Adolescents, and Young Adults in the Post-Vaccine Licensure Era Pediatrics, May 1, 2009; 123(5): e820 - e828. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Marin, H. C. Meissner, and J. F. Seward Varicella Prevention in the United States: A Review of Successes and Challenges Pediatrics, September 1, 2008; 122(3): e744 - e751. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. S. Chaves, P. Gargiullo, J. X. Zhang, R. Civen, D. Guris, L. Mascola, and J. F. Seward Loss of Vaccine-Induced Immunity to Varicella over Time N. Engl. J. Med., March 15, 2007; 356(11): 1121 - 1129. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. T. D'Angio, P. A. Boohene, A. Mowrer, S. Audet, M. A. Menegus, D. S. Schmid, and J. A. Beeler Measles-Mumps-Rubella and Varicella Vaccine Responses in Extremely Preterm Infants Pediatrics, March 1, 2007; 119(3): e574 - e579. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. M. Davis, M. Marin, A. E. Cowan, D. Guris, and S. J. Clark Physician Attitudes Regarding Breakthrough Varicella Disease and a Potential Second Dose of Varicella Vaccine Pediatrics, February 1, 2007; 119(2): 258 - 264. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
