Strategy

The strategy developed by the PAHO rests on the full implementation of three vaccination recommendations that seek to achieve and sustain a high level of vaccine‐induced measles immunity in the population. The strategy is complemented by a sensitive surveillance system capable of timely detection of suspected measles circulation, the confirmation and thorough investigation of all cases, and an effective virologic surveillance system [2, 3, 5].

In the absence of vaccination, ⩾95% of the population of most countries will already have been infected with measles by age 15. Because natural measles infection causes lifelong immunity, a large majority of persons worldwide who are ⩾15 years of age should be immune to measles [7]. Therefore, PAHO recommends a strategy that seeks to rapidly interrupt the transmission of measles by means of an initial mass‐vaccination campaign (catch‐up) for all children aged 9 months to 14 years. The interruption of transmission is maintained through a high degree of population immunity, which is provided by vaccination of children ⩾12 months of age in the routine vaccination services (keep‐up) and complemented with mass‐vaccination campaigns every 4 years (follow‐up), in which all children ages 1–4 years are targeted regardless of previous vaccination status [5]. The aim of this second vaccination opportunity is, first and foremost, to deliver the first dose to those children who never received any measles vaccination and to deliver a second dose to all children who previously received a first dose, thus reaching those who had a primary vaccine failure. PAHO recommends reaching 95% coverage in all catch‐up, keep‐up, and follow‐up vaccination activities in every municipality of the countries. Maintaining high coverage in all municipalities is fundamental to avoid leaving pockets of susceptible children who may allow the reestablishment of transmission.

Because of the need to obtain and maintain uniformly high coverage, this strategy has been complemented by the use of mop‐up vaccinations (which target pockets of unvaccinated children, especially in underserved urban areas and hard‐to‐reach rural areas) following catch‐up and follow‐up measles vaccination activities. Mop‐ups usually include the same age group that was targeted in a mass campaign. High‐risk areas are generally selected on the basis of house‐to‐house monitoring of vaccination coverage from the mass campaign. However, other criteria have been used that include official coverage figures, cases of measles within the last 3 months, poor measles surveillance, deficient access to health services, and large concentrations of urban poor, especially with important populations of migrants of rural origin.

On the basis of results from outbreak investigations in the Americas, PAHO has also targeted the vaccination of population groups considered at high‐risk for sustaining measles transmission and for transmitting measles to susceptible persons of other groups. These groups have included health care workers, young adults who migrate from remote rural areas with low population densities to urban areas and who, thus, may have escaped both natural measles infection and vaccination, and young adults in closed settings.

Measles Cases

Thirty‐nine (95%) of 41 countries reporting to PAHO in the Region have conducted catch‐up vaccination campaigns during 1989–1995 and follow‐up measles vaccination campaigns every 4 years. Routine (keep‐up) vaccination coverage in the Region has increased from 80% in 1994 to 94% in 2000. Measles vaccination coverage for 2000 by country ranged between 75% and 99%. Lowest reported coverage rates were from Colombia (75%), Haiti (80%), Belize (82%), Venezuela and Costa Rica (84%), Guyana (86%), and Jamaica and Dominican Republic (88%) (table 1). Measles vaccination coverage for 2001 by country ranged between 53% and 99%. The lowest reported coverage rate was from Haiti (53%); all others had reported coverage above 80% (table 1).

The age group most susceptible to measles infection remained children <5 years of age, followed by young adults, especially rural migrants and those living in certain institutional settings that can facilitate measles transmission when measles virus is introduced (e.g., army barracks, schools, and prisons). Low vaccination coverage is the main cause for the high attack rate among children <5 years of age, and reduced measles circulation in the areas where they grew up is a major reason for susceptibility among some groups of young adults.

Most countries in the Region consistently have carried out follow‐up vaccination at least every 4 years; however, the timing of such follow‐up is based on the vaccination coverage obtained among infants during routine services since the last campaign. Guatemala, for example, moved its follow‐up measles vaccination campaign from 2003 to early 2002 as a result of an analysis of recent vaccination coverage levels for children <1 year of age, which identified the border areas with Mexico at high risk for a measles outbreak [8].

Virus isolates obtained from outbreaks in the Region since 1997 (including urine specimens from Argentina, Brazil, Bolivia, Chile, Dominican Republic, Haiti, and Uruguay) have all been genotype D6, which indicates that it continued to circulate endemically in the Region since the 1997 São Paulo outbreak. It is unknown if these viruses were introduced to Brazil by importation or if they represented continuous circulation of viruses indigenous to Brazil. Measles viruses belonging to genotype D6 have been isolated in various European countries, but viruses indistinguishable from the D6 viruses isolated during the São Paulo outbreak were responsible for sporadic measles cases for at least 2 years before the outbreak [9]. In Venezuela in 2001, indigenous transmission was re‐initiated after re‐introduction of measles from Europe [10]. The virus genotype is still under investigation.

In 1998, there were 14,332 confirmed cases of measles reported from 17 (41%) of the 41 countries that report to PAHO. Argentina (10,229 cases), followed by Brazil (2781 cases), had the highest number of cases. During January 1999 through December 2000, 28 (68%) of 41 countries that report to PAHO, including Cuba, the English‐speaking Caribbean countries, and most of Central and South America, reported no measles cases. In 1999, 3209 confirmed cases were reported from 11 countries, 78% fewer cases than in 1998 and 94% fewer than in 1997 (figure 1). In 1999, indigenous transmission occurred in four countries: Bolivia (1441 cases), Brazil (908), Argentina (313), and Dominican Republic (274) (figure 2). Also in 1999, Canada, Chile, Costa Rica, Mexico, Peru, Uruguay, and the United States reported measles importations, but secondary transmission was limited as a result of high measles vaccination coverage. The largest outbreak linked to measles importation occurred in Canada, where 165 confirmed cases were linked to an importation from Bolivia.

In 2000, the number of confirmed cases of measles in the Americas decreased to 1754 (figure 1). Indigenous transmission still occurred in Argentina, Brazil, Bolivia, Dominican Republic, and Haiti (figure 2) [3, 11]. Only 16 (<1%) of the 12,010 reporting municipalities in the Region reported confirmed measles cases during this period [12].

During 2001, 537 confirmed measles cases were reported in the Americas. Indigenous transmission was reported in only three countries, Haiti and Dominican Republic (on Hispaniola island) and Venezuela. Dominican Republic’s last confirmed case occurred in June 2001, and Haiti’s last case was reported in September. From August through December 2001, 109 measles cases were reported in Venezuela following an importation from Europe. Since September 2001, Venezuela is the only country with known indigenous transmission in the Region.

Measles in Countries with Indigenous Transmission during 2000–2002

Argentina.  The 1997 measles outbreak in São Paulo spread to Argentina, where a total of 10,673 confirmed cases were reported during the years 1997–2000. Hardest hit were unvaccinated infants and preschool children. Of the outbreak cases, 10,229 (96%) occurred in 1998 and 313 (3%) in 1999. Cases decreased after a 1998 follow‐up measles vaccination campaign, which reported 98% coverage, among children aged 1–4 years. During 2000, 6 confirmed cases were reported, a 99% decrease since 1999. All 2000 cases occurred during February and March in the central province of Cordoba, and all but 1 occurred among unvaccinated persons. Three of the cases were adults (ages 23, 25, and 32 years), and 2 were health care workers. No additional cases have been reported since.

Brazil.  Following the 1997 epidemic (52,284 confirmed cases, 97% of the Region’s total), a national follow‐up vaccination campaign was conducted in Brazil. As a result of this campaign and mop‐up vaccination, reported cases decreased to 908 in 1999 and to 36 in 2000. Of the cases occurring in 2000, 15 (42%) originated from an outbreak in the western Amazon region, possibly related to an outbreak in Bolivia, 12 (57%) were sporadic laboratory‐confirmed cases from São Paulo, and 9 were sporadic cases from other states. In June 2000, a national follow‐up vaccination campaign was conducted targeting children ages 1–11 years and resulted in a reported 100% nationwide coverage. During 2001 and 2002, only 1 case was confirmed per year; both were importations from Japan. Thanks to important efforts in surveillance, the data have improved in timeliness and sensitivity during the past 2 years. Analysis of these data indicates that indigenous measles transmission was interrupted in 2000. This achievement was the result of Brazil’s intensive efforts to reach high routine vaccination coverage during 1999–2000, successful implemention of a national follow‐up vaccination campaign, and adequate outbreak investigations and timely and efficient mop‐up operations in areas where transmission was confirmed (table 1).

Bolivia.  In 1999, 1441 confirmed measles cases (45% of the Region’s total) were reported in Bolivia, representing a 44% increase from the 1004 cases reported in 1998. The measles outbreak began in May 1998, spreading from Yacuiba on the Argentinean border to all regions of the country. A follow‐up measles vaccination campaign was carried out during November and December 1999, with reported national coverage of 98%. However, house‐to‐house monitoring indicated that most areas had not achieved 95% coverage during the campaign.

In 2000, 122 measles cases were reported in five outbreaks affecting rural, unvaccinated children and young unvaccinated adults who had migrated from rural areas. The largest outbreak (66 cases) occurred during March through June 2000 in a Mennonite community in Santa Cruz that objects to vaccination for philosophical reasons [13]. This outbreak was identified after a measles outbreak was reported from a related community in Alberta, Canada. Members of this community had traveled to a Mennonite community in Santa Cruz. From September through December 2000, a nationwide, house‐to‐house vaccination campaign was implemented to administer all vaccines used in the routine vaccination schedule for infants (diphtheria–tetanus toxoids–pertussis, measles, mumps, and rubella, and oral poliovirus vaccines). To supervise the campaign, measles vaccination coverage was monitored house‐to‐house in most municipalities, and those that failed to reach the required 95% coverage were requested to vaccinate again. No additional cases have been confirmed since then. Tools for rapid monitoring of vaccination coverage following vaccination, together with active‐case search at municipalities that were active, silent, or in border areas or that had migrant populations, and the deployment of special rapid response teams for mop‐up vaccination in high‐risk municipalities proved critical in controlling the epidemic.

Ecuador.  In May 2001, after 3 years with no confirmed cases of measles, 2 serologically confirmed cases were reported in Quito, Ecuador, but no specimens were available for virologic analysis. No additional cases were found during an active‐case search that was conducted nationally during June through August 2001. No cases have been confirmed since then.

Dominican Republic.  In 2000, there were 274 confirmed measles cases reported in 1999 and 253 (14% of the Region’s total) in Dominican Republic. Highest attack rates in 2000 occurred among children <5 years of age (with rates ranging between 2/100,000 for children aged 1–4 years to 32/100,000 for children aged 6–11 months). Children aged 5–9 years and young adults aged 20–29 years also had high incidence rates (2/100,000). During 2001, a total of 113 cases (21% of the Region’s total) were confirmed from 18 provinces. The last case was confirmed on 9 June (epidemiologic week 23). A nationwide measles and polio vaccination campaign was implemented during May 2001. Average vaccination coverage validated by house‐to‐house monitoring was 94%. The decision to vaccinate against measles starting at 6 months of age played a major role in reducing the incidence of measles among infants <1 year of age. Concurrent mop‐up vaccination among workers in areas identified as high risk (free‐trade zones, health care settings, hotels, tourist services) also contributed to the interruption of measles transmission among persons 20–29 years old.

Haiti.  In 1994, Haiti completed a nationwide catch‐up vaccination campaign against measles, resulting in an estimated official vaccine coverage of >95% among children 9 months to 14 years of age. Following this campaign, Haiti remained free of measles for 6 years. Since then, the level of routine immunization has been low, with measles vaccine coverage among 1‐year‐old children averaging 47% (range, 32%–85%) between 1995 and 1999. This led to an accumulation of >1 million susceptible children below the age of 5 years. A follow‐up measles vaccination campaign was conducted in 1999, but failed to reach the target population of all children <5 years of age (∼1.3 million children). Estimated coverage was between 70% and 80%. The main reasons for the suboptimal results of the campaign included lack of political will, failure to closely supervise vaccinators, and logistical failures in delivering vaccine on time and in good condition. As a result, Haiti was at risk for a new measles epidemic, and Dominican Republic, which shares the island of Hispaniola with Haiti and receives thousands of visitors and immigrants from Haiti every year, was experiencing a large measles outbreak that began in June 1999.

In 2000, a measles outbreak due to an importation from Dominican Republic began in Artibonite. Between November and December 2000, a house‐to‐house vaccination campaign was implemented in Delmas, Port au Prince, the most affected neighborhood of the country. The total number of cases for 2000 was 992 (55% of the Region’s 1754 cases). During 2001, a total of 159 confirmed cases (30% of the Region’s total) was confirmed. Most cases occurred among children <5 years of age, with the highest incidence among children 6–11 months old (34/100,00), followed by children aged 1–4 years. Between September and November 2001, Haiti carried out a nationwide follow‐up measles vaccination campaign that, according to official figures, reached over 100% vaccination coverage. House‐to‐house monitoring showed that ∼92% of the children interviewed had been vaccinated. The last confirmed case was reported on 26 September (epidemiologic week 39) 2001.

Venezuela.  During 2000, an outbreak of 22 confirmed cases among preschool and school‐age children occurred in Zulia, Venezuela, a highly populated northwestern state bordering Colombia. Because of delays in the reporting and investigation of the outbreak and because of the lack of viable specimens, the origin of the outbreak remains unknown. A nationwide active‐case search performed during the first semester of 2001 identified a total of 8 suspected cases that had not been previously reported and for which no serum samples were available. Given the lack of sufficient information, these 8 cases were defined as clinically confirmed measles cases.

In September 2001, a measles outbreak started in the state of Falcon, Venezuela, after an importation from Europe by a 35‐year‐old man (figure 2). The outbreak spread to Zulla, the country’s most populous state. From September to December 2001, 109 cases were confirmed in these 2 states. During 2002, the outbreak spread to 17 (63%) of the country’s 27 states, with a total of 2392 cases in 2002. Only 18% of the total confirmed patients had been vaccinated with a measles‐containing vaccine. The case incidence by age shows that the highest incidence (122/100,000) occurred among children aged <1 year, followed by children aged 1–4 years (27/100,000) and young adults aged 20–29 years (12/100,000). A nationwide vaccination campaign that included both children and young adults was initiated in November 2001. During 2002, house‐to‐house monitoring was used by supervisors to assess the quality of the vaccination effort at the local level. The last case of the outbreak occurred on 16 November 2002 in the state of Carabobo. No other confirmed indigenous measles cases have been reported in the Region of the Americas since then.

Colombia.  On 20 January 2002, a 7‐year‐old girl from Barranquilla was infected with measles after a visit to Maracaibo, Venezuela (figure 2). The outbreak spread to a total of 11 (33%) of the 33 departments of Colombia, with a total of 140 confirmed cases. A nationwide measles vaccination campaign, which started in the departments bordering Venezuela, was implemented. The last 3 cases occurred on 12 September 2002 in the departments of Bolivar, Cundinamarca, and Magdalena. No additional confirmed measles cases have since been reported from Colombia.

Discussion

Measles is a highly infectious disease that carries significant mortality. The outbreaks in Brazil and Argentina have demonstrated the lethality of measles virus. Over 100 measles‐related deaths, mostly among unvaccinated infants and preschool‐aged children, were reported during the 1997–1998 outbreaks in these two countries. The high incidence among 6‐ to 11‐month‐old children, mainly due to waning of maternal immunity, is also a reason for concern because young children carry a higher risk for hospitalization and death [7]. The impact of measles vaccination on child survival, particularly among the poor, has been reiterated in a recent study showing that vaccination of poor children significantly improves their long‐term chances for survival [14].

As a result of intensified vaccination efforts guided by surveillance activities and active‐case searches in health centers, schools, and high‐risk communities, the incidence of measles as of December 2001 was reduced >99% compared with the incidence in 1999. Moreover, as of January 2003, no known indigenous measles transmission had occurred in the Region since November 2002. This unprecedented success is due to the total commitment of all governments in the Region with the goal of measles eradication and to their compliance with PAHO’s recommendations. This is even more impressive if we account for the fact that the sensitivity of measles surveillance in the Region has continuously improved since 1990.

Still, measles case surveillance data combined with molecular epidemiology information provided by PAHO’s measles laboratory network shows the constant threat of importation of measles virus from other regions where the disease remains endemic. An importation of measles virus triggered outbreaks in 1998 and 1999 in Argentina, Bolivia, and Dominican Republic, the 2000–2001 outbreak in Haiti, and the 2001–2002 outbreak in Venezuela and Colombia. These introductions were successful in reinitiating indigenous transmission because they found large groups of susceptible populations as a result of the failure to fully implement PAHO’s recommended vaccination strategy. In 2001, São Paulo, the most densely populated city in Brazil, had a measles importation from Japan, which did not disseminate because of Brazil’s successful efforts to achieve high vaccination coverage during 1999–2000. The finding of this importation was due to the strengthening of the timeliness and sensitivity of measles surveillance. The efforts of El Salvador in reaching measles coverage rates above 95% were also instrumental in preventing the resurgence of indigenous measles virus in this country when two importations from Europe occurred in May 2001. The outbreak in Venezuela illustrates, however, the dangers of failing to maintain high routine vaccination coverage.

The full implementation of PAHO’s recommended strategy in all countries remains the keystone of our efforts toward the interruption of indigenous measles transmission. Countries that have failed to either conduct timely follow‐up vaccination campaigns or to sustain high levels of vaccine‐induced measles immunity have experienced large outbreaks following measles introduction. Countries maintaining high population immunity and a sensitive measles surveillance system have experienced measles importations without resumption of indigenous measles transmission.

Recommendations for countries in the Americas call for maintenance of the highest population immunity among infants and children while targeting adolescents and young adults at highest risk of exposure for special vaccination efforts. Lessons learned from the outbreaks in the Americas have also highlighted the importance of susceptible young adults in disease introduction and dissemination. Young adults, particularly those recently migrating to urban areas, are a risk factor for measles virus transmission in Brazil and were implicated in spreading the disease to other areas in most outbreaks that occurred in the Americas. PAHO’s 1999 and 2000 Technical Advisory Group meetings on Vaccine Preventable Diseases addressed this concern by issuing a recommendation to vaccinate special at‐risk groups as determined on the basis of each country’s epidemiologic situation [15, 16].

Experience gained in the Americas during the past 6 years has pointed toward the need to validate the measles vaccination effort at the lowest geographic level through house‐to‐house monitoring and to identify localities with persistent low vaccination coverage within countries that report an adequate level of aggregate coverage. During the outbreaks in Bolivia and Haiti, supervisory tools were developed to improve the assessment of vaccination and surveillance efforts at the local level. These tools have now become instruments of routine supervision in those countries. PAHO’s efforts in 2001 have been aimed toward standardizing supervisory tools for vaccination coverage, investigating measles outbreaks, and validating routine surveillance. The routine verification of the quality of vaccination and surveillance efforts through monitoring and active‐case searches has become critical in preventing countries from developing a false sense of security based on overestimated coverage and insufficient surveillance.

Experience in the Region has also shown that house‐to‐house vaccination is the most efficient strategy for achieving high and homogenous coverage in high‐risk and hard‐to‐reach areas. This was particularly evident in Haiti and Bolivia, where door‐to‐door vaccination became necessary to reach the target coverage levels needed to achieve the interruption of indigenous measles transmission.

The implementation of PAHO’s strategies has also raised the attention of policy‐makers in regard to equity issues. One example is the case of seasonal rural workers in Bolivia identified as high‐risk groups for measles virus transmission during the 1998–2000 outbreak. These workers had practically no access to any health or education services. Another critical issue raised by the measles experience is the case of the Mennonite groups in Bolivia who resisted vaccination for philosophical reasons. During a measles outbreak investigation among the Mennonites, health authorities of Santa Cruz identified them as one of the least vaccinated groups in the country. Following frequent visits and dialogue, the Mennonites were persuaded to accept vaccination. As a result of these efforts, measles vaccination coverage among the Mennonites became the highest (98%) of any group in the country in 2000.

The main added value of the measles initiative in the Americas has been its contribution to improvements in technical and managerial capabilities and the increased responsibility and accountability of public health staff in charge of immunizations at the local, provincial, and national level in all countries of the Region. The priority being given to regular supervision and increased accountability through house‐to‐house monitoring of vaccination coverage, active‐case search, and improvements in surveillance and case investigation have been fundamental in strengthening the planning and implementation of routine immunization services at the local level. The same applies to the significant improvements made in cold‐chain equipment maintenance and supervision during measles vaccination efforts in various countries. The continued high‐level commitment of health authorities to immunization, which began during the polio eradication years in the Americas, remains an example to the world. Sustained political, financial, and social commitment and sound strategies have made the interruption of indigenous measles transmission in the Americas an achievable goal.