IJE Advance Access originally published online on December 15, 2008
International Journal of Epidemiology 2009 38(1):182-191; doi:10.1093/ije/dyn261
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Ongoing measles and rubella transmission in Georgia, 2004–05: implications for the national and regional elimination efforts
1 Epidemic Intelligence Service Program, Career Development Division, Office of Workforce and Career Development, Centers for Disease Control and Prevention, Atlanta, GA USA.
2 Global Immunization Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA USA.
3 Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA USA.
4 National Center for Disease Control, Tbilisi, Republic of Georgia.
5 Present address: Preventive Medicine Residency Program, Career Development Division, Office of Workforce and Career Development, Centers for Disease Control and Prevention, Atlanta, GA USA.
* Corresponding author: CDC, 1600 Clifton Rd., Mailstop E-05, Atlanta, GA 30333, USA. E-mail: auzicanin{at}cdc.gov
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Abstract |
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Background In 2004–05, Georgia experienced large-scale concurrent measles and rubella outbreaks. We analysed measles and rubella epidemiology in Georgia to describe disease trends, determine the cause of the outbreaks, identify challenges to achieving disease elimination goals and propose interventions to overcome them.
Methods We reviewed national measles and rubella surveillance and vaccination coverage data, focusing on the 2004–05 outbreaks, and conducted a measles vaccine effectiveness (VE) study using data from a 2004 school-based outbreak.
Results Before 2004, the last large measles outbreak after measles vaccination was introduced (in 1966) in Georgia, was in 1988 (incidence rate, 36/100 000); the highest year for rubella was 1985 (110/100 000). During 2004–05, 8391 measles cases and 5151 rubella cases were reported (most of them diagnosed clinically). Of 358 suspected measles cases tested, 181 (51%) were positive for measles-IgM antibody; of 240 suspected rubella cases tested, 50 (21%) were positive for rubella-IgM antibody. Over 90% of measles cases were in persons born after 1979; 90% of rubella cases were in persons born after 1987. Approximately 41% of measles cases and 88% of rubella cases were unvaccinated. Estimated measles VE (
1 vs 0 doses) was 86% (95% CI, 58–96%).
Conclusions The outbreak likely resulted from failure to vaccinate rather than vaccine failure. Susceptible persons likely accumulated due to the long absence of large outbreaks and decreased coverage after the collapse of Soviet Union. To interrupt measles and rubella transmission in Georgia and achieve disease elimination goals by 2010, supplementary immunization activities should target children and young adults.
Keywords Measles, rubella, outbreaks, Georgia
Accepted 6 November 2008
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Background |
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The European Region of the World Health Organization (WHO/EURO) has targets for eliminating indigenous measles and rubella by 2010.1 However, despite a predominance of two-dose routine immunization programmes in the Region, measles outbreaks continue to occur.2–4 Former Soviet Union republics, particularly Georgia, independent since 1991, face substantial difficulties achieving these targets due to political, economic and infrastructural challenges after gaining the independence.5,6
Georgia (population 4.6 million)7 adopted the WHO/EURO goals for measles and rubella elimination in 2002. In this paper, we used national surveillance data to describe measles and rubella epidemiology in Georgia, emphasizing the large-scale concurrent measles and rubella outbreak in 2004–05. This information was used to identify specific challenges to achieving disease elimination goals in Georgia and propose optimal approaches to help overcome them.
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Methods |
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We reviewed historic data on Georgia's national immunization policy and vaccination coverage and national surveillance data on measles (from 1958) and rubella (from 1980) incidence, available at the National Center for Disease Control (NCDC) in Tbilisi, Georgia. We also reviewed laboratory data at the NCDC National Measles and Rubella Laboratory (NMRL) and cross-checked them with the surveillance data.
In Georgia, WHO measles and rubella surveillance guidelines for public health services, clinicians and laboratorians were introduced in 2004.8 Prior to this, cases were reported based on clinical diagnosis only. Case-based surveillance for these diseases has been in place since 2004. Laboratory confirmation has been available at NMRL since 2004 using a commercial enzyme-linked immunoassays for measles and rubella IgM antibodies (Dade Behring, Marburg, Germany). Reported cases are tested for measles and/or rubella-IgM antibodies depending on clinical suspicion and if the health care provider requests confirmation. Congenital rubella syndrome (CRS) surveillance has been in place since 1996, but its awareness among health care providers is very limited.
Case-based reporting forms included district/region, dates of patient's birth and illness onset, immunization status, laboratory confirmation, outcome, hospitalization status, complications, pregnancy status (for rubella) and final classification. Data from the forms for 2004–05 were analysed using Epi Info Version 3.3.2 (CDC, Atlanta, GA).
Incidence rates were calculated per 100 000 population using data from the State Department of Statistics. Age-specific attack rates were calculated according to the age-groups for which age-specific population data were available.
A retrospective cohort study to estimate measles vaccine effectiveness (VE) was conducted using data from a 2004 school-based outbreak in Dzalisi village (Mtskheta-Mtianeti region). The school catchment area is limited to this village, and the village clinic is the sole provider of primary health care, including immunizations, to all children in the village. Therefore, we were able to obtain from the clinic the list of all children enrolled in school in 2004 (1988–98 birth cohorts). Measles immunization status was included in the medical records but information on previous history of measles was not available. The list of reported measles cases was obtained from the local District Public Health Center. VE was calculated using the following formula: VE = [1 – (ARvaccinated/ARunvaccinated)] x 100,9 and 95% confidence intervals (CI) were calculated using the EpiTable programme in Epi Info version 6.04 (CDC, Atlanta, GA).
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Measles and rubella immunization policies and coverage
Georgia introduced routine childhood measles vaccination in 1966 as a single dose of Soviet-produced monovalent vaccine at 15 months of age. Subsequent changes to the measles vaccination schedule are depicted in Table 1. Routine two-dose measles-mumps-rubella vaccine (MMR) vaccination began in 2004; routine childhood rubella vaccination did not exist previously in Georgia. Measles vaccination coverage data available from 1980, including MMR coverage from 2004, are presented in Table 2.
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Incidence of measles and rubella
In the pre-vaccine era measles was highly endemic in Georgia, with incidence rates as high as 729 per 100 000 in 1965 (Figure 1). Inter-epidemic intervals were
2–3 years with the highest peaks observed in 1960 and 1965. After vaccine introduction, the magnitude of epidemic peaks steadily declined and the inter-epidemic intervals increased with the last major outbreaks in 1981, 1983 and 1988. A large measles outbreak did not occur again until 2004 (rate, 163/100 000). This outbreak continued into 2005, although the incidence rate dropped to 31/100 000. According to subsequent surveillance data, the rate further declined to 7.5/100 000 (334 cases) in 2006 and 1.0/100 000 (44 cases) in 2007.
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The peak incidence years for rubella before 2004 were in 1983 (60/100 000), 1985 (110/100 000), 1988 (78/100 000) and 1997 (53/100 000) (Figure 1). Concurrent measles and rubella outbreaks occurred in 1983 and 1988. During 2004–05, a large-scale rubella outbreak with rates of 97/100 000 in 2004, and 43/100 000 in 2005, coincided with a large measles outbreak. Subsequently, rubella incidence in Georgia declined to 10.8/100 000 (482 cases) in 2006 and 5.1/100 000 (225 cases) in 2007.
Measles epidemiology during the 2004–05 outbreak
Overall, 8391 measles cases were reported during 2004 (7033 cases) and 2005 (1358 cases) (Figure 2). Most cases were diagnosed clinically. Of 358 suspected cases tested for measles-IgM antibody, 181 (51%) were laboratory-confirmed. The most common reasons for testing were suspected measles and differentiation between measles and rubella (Table 3).
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Case-based data were available for 5988 (85.1%) measles cases in 2004 and 986 (73%) measles cases in 2005. Cases were reported from all regions of Georgia. The completeness of case-based reporting (percentage of case-based reports from the total number of reports) varied among regions, but remained at
80% for 8 of 12 regions. The subsequent analyses are based on the 6974 reports with case-based information available. Demographic characteristics of measles cases during 2004 and 2005 are given in Table 4. Cases occurred across a wide age range (0–69 years) with a median age of 13 years during both 2004 and 2005. More than 85% of cases during 2004–05 occurred among persons born after 1983, with the 1985–97 birth cohorts accounting for 58.2% of cases (Figure 3). Eleven per cent of cases occurred among children born in 2003–05, with 6.2% aged <1 year. For both 2004 and 2005, the highest age-specific incidence rate was observed in children aged <1 year (773 and 159 per 100 000, respectively). The next highest age-specific rate for both years was in children aged 10–14 years (507/100 000 in 2004, 56/100 000 in 2005).
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In 2005 compared with 2004, the proportion of 10- to 14-year old cases declined (from 29% in 2004 to 19% in 2005; P < 0.001) and the proportion of cases aged >15 years increased (from 37% to 46%, respectively; P < 0.001) (Table 4). In terms of the proportion of cases attributable to individual birth cohorts, the greatest decline in 2005 vs 2004 was experienced by the children born in 1990–92 (from 20% to 11%, P < 0.001) and in 2000–01 (from 5.5% to 3.6%; P < 0.05) (Figure 3). The 1990–92 birth cohorts were the ones most affected by the disruption of health services immediately after the independence, and children born in 2000–01 were the first birth cohorts to receive the routine dose of MMR2.
Unvaccinated persons accounted for >40% of cases in both 2004 and 2005 (Table 4). Among 2827 vaccinated case-patients (41% of total), 402 (14%) received two doses and 2425 (86%) were single-dose recipients. The proportion of 1-dose recipients declined from 36% in 2004 to 25% in 2005 (P < 0.001), the proportion of two-dose recipients remained unchanged, and the proportion of cases with unknown vaccination status, >70% of which were among persons aged 15 years, increased (27% vs 17%; P < 0.001).
Various complications of measles were reported for 796 (11%) cases (Table 4). The most commonly reported complications, pneumonia and encephalitis, accounted for 72% (570 cases) and 9% (77 cases) of all complications, respectively. Hospitalization was required for 19% of reported measles cases, including 554 (70%) cases with reported complications. Unvaccinated persons had higher risk of hospitalization [relative risk (RR), 2.6; 95% CI, 2.3–2.9] and complications (RR, 2.1; 95% CI, 1.8–2.5), than vaccinated persons. When compared with 5- to 14-year olds, the age group with the lowest proportion of hospitalized cases (10.5%), the risk of hospitalization was highest for adults aged 20 years (35.2%; RR, 3.4; 95% CI, 3.0–3.8) and children <1 year of age (29.5%; RR, 2.8; 95% CI, 2.4–3.4).
Nine measles deaths were reported (overall case-fatality ratio, 0.1%). Five deaths occurred among children aged 
1 year, and four were among adults aged >18 years. Five (56%) of the fatal cases were unvaccinated, one had received one dose of measles containing vaccine (MCV), one had two doses of MCV, and for two adult cases, vaccination status was unknown.
Rubella epidemiology during the 2004–05 outbreak
In 2004, 4209 rubella cases were reported compared with 1842 in 2005 (Figure 2). Most cases were diagnosed clinically. Of 240 suspected cases tested for rubella-IgM antibody, 50 (21%) were laboratory-confirmed (Table 3). Case-based data were available for 699 (16.6%) rubella cases in 2004 and for 1531 (83.2%) rubella cases in 2005. In 2004, case-based data were reported from 2 of 12 regions—Imereti, which was the site of a pilot surveillance project and accounted for 99.3% of the case-based rubella data for the year, and Samtskhe-Javakheti. All regions reported case-based rubella data in 2005, with 45% of cases reported from Tbilisi and 16% from Imereti.
Characteristics of rubella cases in 2004–05 are given in Table 5. The median age of cases was 9 years (range, 0–52 years). Age-specific incidence rates were highest for children aged 5–9 years (67/100 000 in 2004 and 164/100 000 in 2005), followed by those aged 10–14 years in 2004 (64/100 000) and 1–4 years in 2005 (127/100 000). Cases most commonly occurred among children born during 1993–1997 (40.1% of all cases) and >90% occurred among those born in or after 1988 (Figure 4). Women of childbearing age (15–44 years) accounted for 167 (7.5%) cases, including nine cases among pregnant women (five laboratory-confirmed). Pregnancy outcome data for these women were not available.
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Unvaccinated persons accounted for 1962 (88%) reported rubella cases (Table 5), including all 36 (2%) hospitalized cases. Hospitalized cases, including one laboratory confirmed case, occurred among persons aged 1–33 years with 21 (58%) aged <15 years. There were no reported rubella deaths. No CRS cases were reported in Georgia during 1996–2003 and only three cases were reported thereafter.
Measles VE assessment
Of the 386 children enrolled at the school in Dzalisi village during the 2004 outbreak, immunization history was available for 349 (90.4%), including all 13 measles cases (all clinically diagnosed) among the students. Of the 349 children with known vaccination history, 337 (96.6%) had received 1 dose of MCV, including 221 (66.3%) 1-dose recipients, and 116 (33.2%) two-dose recipients. Twelve (3.4%) children were unvaccinated. Since 12 of 13 cases occurred among children born during 1988–93, the calculation of attack rates and VE was limited to these birth cohorts. Coverage with 1 dose of MCV was similar between the birth cohorts 1988–93 and 1994–98 (95.7% vs 97.9%, P > 0.05), but two-dose coverage was lower among those born in 1988–93 than among those born in 1994–98 (24.5% vs 46.1%, P < 0.0003).
The risk of measles was higher among the unvaccinated children than among recipients of 1 dose of MCV (RR, 7.4; 95% CI, 2.4–22.7). VE of 1 dose vs 0 doses was 86.4% (95% CI, 58.3–95.6), with no difference between single-dose recipients compared with two-dose recipients (Table 6).
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Discussion |
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From 1988 through 2004, measles epidemiology in Georgia was characterized by low reported incidence and virtual absence of larger outbreaks, likely as a result of a successful routine measles vaccination programme in place since 1966. However, due to incomplete measles vaccination coverage which further declined during the 1990s, and the absence of rubella vaccination programme until 2004, measles and rubella viruses continued to circulate in Georgia leading to the large-scale measles and rubella outbreak in 2004–05.
The outbreak affected all geographic regions and a wide age range. There was a substantial overlap in clinical presentations and affected age groups between the two diseases, and laboratory confirmation of suspected cases was rarely sought. Failure to vaccinate rather than vaccine failure was the primary cause of the outbreak.
Large groups of persons susceptible to measles across a wide age range accumulated in Georgia due to the disruption of immunization services following the collapse of the Soviet Union and suboptimal coverage immediately prior to and in the early years of independence.5,6 The resulting inadequate vaccination coverage,10 combined with the absence of large scale measles outbreaks since 1988, likely contributed to this measles outbreak.
The majority of measles cases were among school-age children and young adults, with >75% of cases occurring among unvaccinated persons and 1-dose recipients of measles vaccine. The focus of the measles outbreak was in cohorts born around the time of collapse of the Soviet Union, who have been most affected by the 1990s disruption in routine vaccination services. The high incidence rates of measles among children <1 year of age resulted from an increased risk of measles transmission to unprotected infants during a large outbreak and the lack of maternal immunity because many mothers were neither vaccinated nor exposed to natural infection prior to becoming pregnant.11,12
The substantial incidence of measles among young adults and the changes in vaccination status of measles cases over time are consistent with the history of immunization practices in Georgia. Following the initial reasonably high vaccination coverage, there was a period in the 1990s when routine doses were either delayed or not administered due to interruptions in vaccine availability and general disruption of health services. In an attempt to address the inadequate coverage, nationwide implementation of the second dose of measles vaccine along with the supplementary immunization activities (SIAs) for the birth cohorts of 1990–96 was undertaken, but as shown by this investigation, these measures were not sufficient to prevent the outbreak.
The analysis of the measles surveillance data and the VE assessment demonstrated vaccine-associated protection against the disease, complications and hospitalization, as well as the greatest decline in measles incidence for the birth cohorts targeted by SIAs or routine MMR2, suggesting that overall effectiveness of the measles vaccination programme in Georgia is high. However, the VE results cannot be generalized to the whole country as this district may not be representative of all of Georgia. Also, the lack of information on previous measles infections among the students could have introduced a bias towards increasing the VE estimate. In addition, all cases in the VE study were clinically diagnosed without laboratory confirmation. Nevertheless, taken together, the data from the outbreak epidemiology and VE study support that the current measles transmission in Georgia is a result of failure to vaccinate with two-doses MCV rather than vaccine failure.
In 2004, Georgia had the highest measles incidence rate among all countries of the WHO/EURO.1 However, several other countries in the region, including Romania, Ukraine, Germany, Italy and Ireland, also experienced large measles outbreaks around the same time period in spite of routine two-dose vaccination programmes.2–4,13,14 In many of these countries, as with Georgia, the second dose had been recently introduced or coverage was not very high.
The epidemiology of the 2004–05 rubella outbreak in Georgia, which affected predominantly unvaccinated children, was consistent with that of a country without rubella vaccination programme. Because only a small proportion of rubella cases in 2004 had case-based reports, our analysis more accurately reflects the rubella epidemiology in 2005 than 2004.
The major challenge to accurately describing the epidemiology of this concurrent outbreak of measles and rubella lies in the low rates of laboratory testing. Because laboratory confirmation was rarely attempted, misclassification of measles and rubella cases may have occurred, resulting in biased age distribution of reported cases and age-specific incidence rates as well as disease-specific hospitalization rates. A substantial overlap in clinical features, especially for mild cases, coupled with concurrent transmission of both measles and rubella made differential diagnosis on clinical grounds difficult, as evident from the available laboratory data.
In recent years, substantial progress has been made toward improving measles and rubella control in Georgia, including the development and implementation of case definitions and surveillance guidelines, nationwide introduction of case-based reporting, availability of laboratory confirmation, implementation of a two-dose schedule with MMR, an increasing trend in vaccination coverage through improved routine immunization delivery, and the MMR catch-up campaigns among the 1990–92 birth cohorts.
However, considerable challenges remain to fully implementing surveillance and immunization strategies for measles and rubella elimination in Georgia. Surveillance for these diseases, particularly its laboratory component and CSR surveillance, needs to be further strengthened. The implementation of the current national measles and rubella surveillance guidelines was still incomplete during the outbreak, resulting in underreporting and lack of laboratory confirmation. Previous studies have noted that with a two-dose routine vaccination programme, a sustained coverage of 95% with both doses of MCV is necessary to ensure high population immunity needed for measles elimination.15–17 As of 2005, routine childhood immunization programme in Georgia did not reach the target of 95% for either of the two routine doses of MMR.
To prevent future outbreaks and achieve high population immunity needed to interrupt measles and rubella transmission in Georgia, a one-time SIA targeting susceptible population regardless of previous measles/rubella immunization status or disease history is needed. Similar SIAs have been successfully utilized in other European countries and elsewhere.18–20 Given the large concurrent rubella outbreak in 2004–05 with continued transmission, the existing goal of rubella elimination, and the introduction of MMR in Georgia's routine immunization programme in 2004, a combined measles-rubella vaccine should be considered the vaccine of choice for the campaign. The epidemiology of the 2004–05 outbreak and the results of this study suggest that, ideally, all persons born after 1983 should be targeted for the SIA. Special focus on sustaining high levels of immunity to rubella among women of child-bearing age will be needed after the campaign.
The routine measles/rubella vaccination programme should also be further strengthened to achieve and maintain routine coverage of 95% with both doses of MMR. Reintroduction and enforcement of school entry vaccination requirements could help with achieving and sustaining high coverage with all routine vaccinations among school-aged children.21,22 Combined with the SIA, the above measures should help Georgia attain the high population immunity needed to eliminate indigenous measles and rubella.
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Global Immunization Division; National Center for Immunization and Respiratory Diseases; Centers for Disease Control and Prevention, Atlanta, GA, USA.
Conflict of interest: None declared.
KEY MESSAGES
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1 WHO. Eliminating measles and rubella and preventing congenital rubella infection: WHO European Region strategic plan 2005–2010 (2005) Copenhagen, Denmark.
2 Gee S, Carton M, Cotter S. Measles increase in Ireland, 2004. In: Eurosurveillance Weekly (2004) (15 August 2006, date last accessed). 8. http://www.eurosurveillance.org/ew/2004/040923.asp#3.
3 Spika JS, Aidyralieva C, Mukharskaya L, et al. Measles outbreak in the Ukraine, 2005–2006. In: Eurosurveillance Weekly (2006) E060309.1.
4 Siedler A. Measles outbreaks in Hessen and Bavaria, Germany, 2005. In: Eurosurveillance Weekly (2005) (15 August 2006, date last accessed). 10. http://www.eurosurveillance.org/ew/2005/050728.asp#1.
5 Khetsuriani N, Imnadze P, Dekanosidze N, Khetsuriani N, Imnadze P, Dekanosidze N. Diphtheria epidemic in the Republic of Georgia, 1993–1997. J Infect Dis (2000) 181(Suppl 1):S80–85.[CrossRef][Web of Science][Medline]
6 Henderson RH. Immunization: going the extra mile. In: The Progress of Nations: 1998—Way C, ed. (1998) New York: UNICEF. 13–19.
7 Georgia State Department of Statistics. Population Census, 2002 (2002) (8 March 2006, date last accessed). http://www.statistics.ge/main.php?pform=145&plang=1.
8 WHO. Surveillance Guidelines for Measles and Congenital Rubella Infection in the WHO European Region (2003) Copenhagen, Denmark: World Health Organization.
9 Orenstein WA, Bernier RH, Dondero TJ, et al. Field evaluation of vaccine efficacy. Bull World Health Organ (1985) 63:1055–68.[Web of Science][Medline]
10 Gamkrelidze A, Atun R, Gotsadze G, MacLehose L. Health Care Systems in Transition: Georgia (2002) Copenhagen, Denmark: WHO Regional Office for Europe.
11 Marin M, Nguyen HQ, Langidrik JR, et al. Measles transmission and vaccine effectiveness during a large outbreak on a densely populated island: implications for vaccination policy. Clin Infect Dis (2006) 42:315–19.[CrossRef][Web of Science][Medline]
12 Papania M, Baughman AL, Lee S, et al. Increased susceptibility to measles in infants in the United States. Pediatrics (1999) 104:e59.
13 Hennessey KA, Ion-Nedelcu N, Craciun MD, Toma F, Wattigney W, Strebel PM. Measles epidemic in Romania, 1996–1998: assessment of vaccine effectiveness by case-control and cohort studies. Am J Epidemiol (1999) 150:1250–57.
14 Ciofi degli Atti M, Salmaso S. New measles epidemic in southern Italy: 1217 cases reported to sentinel surveillance, January-May 2003. In: Eurosurveillance Weekly (2003) (20 November 2006, date last accessed). 7. http://www.eurosurveillance.org/ew/2003/030703.asp#1.
15 Lynn TV, Beller M, Funk EA, et al. Incremental effectiveness of 2 doses of measles-containing vaccine compared with 1 dose among high school students during an outbreak. J Infect Dis (2004) 189(Suppl 1):S86–90.[CrossRef][Web of Science][Medline]
16 Hutchins SS, Dezayas A, Le Blond K, et al. Evaluation of an early two-dose measles vaccination schedule. Am J Epidemiol (2001) 154:1064–71.
17 Vitek CR, Aduddell MD, Brinton MJ, Hoffman RE, Redd SC. Increased protections during a measles outbreak of children previously vaccinated with a second dose of measles-mumps-rubella vaccine. Pediatric Infect Dis J (1999) 187:620–23.
18 Ramsay ME, Jin L, White J, Litton P, Cohen B, Brown D. The elimination of indigenous measles transmission in England and Wales. J Infect Dis (2003) 187(Suppl 1):S198–207.[CrossRef][Web of Science][Medline]
19 Quiroga R, Barrezueta O, Venczel L, et al. Interruption of indigenous measles transmission in Bolivia since October 2000. J Infect Dis (2003) 187(Suppl 1):S121–26.[CrossRef][Web of Science][Medline]
20 De Quadros CA, Izurieta H, Carrasco P, Brana M, Tambini G. Progress toward measles eradication in the region of the Americas. J Infect Dis (2003) 187(Suppl 1):S102–10.[CrossRef][Web of Science][Medline]
21 Yeung LF, Lurie P, Dayan G, et al. A limited measles outbreak in a highly vaccinated US boarding school. Pediatrics (2005) 116:1287–91.
22 Kolasa MS, Klemperer-Johnson S, Papania MJ. Progress toward implementation of a second-dose measles immunization requirement for all schoolchildren in the United States. J Infect Dis (2004) 189(Suppl 1):S98–103.[CrossRef][Web of Science][Medline]
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