IJE Advance Access originally published online on January 19, 2005
International Journal of Epidemiology 2005 34(3):556-564; doi:10.1093/ije/dyi001
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Published by Oxford University Press 2005
Article |
Migration as a risk factor for measles after a mass vaccination campaign, Burkina Faso, 2002
1 Health Information System, Directorate of Studies and Planning, Ministry of Health, Ouagadougou, Burkina Faso
2 Global Immunization Division, National Immunization Program, Centres for Disease Control and Prevention, 1600 Clifton Road, NE MS-E05, Atlanta, GA 30333, USA
3 Service for Vaccine Prevention, Directorate of Preventive Medicine, Ministry of Health, Ouagadougou, Burkina Faso
4 Office of the World Health Organization Representative, Ouagadougou, Burkina Faso
5 World Health Organization Office for Africa, Vaccine Preventable Diseases, Harare, Zimbabwe
6 Expanded Programme on Immunization, World Health Organization, Geneva, Switzerland
* Corresponding author. Dr Robert Perry, Centres for Disease Control and Prevention, 1600 Clifton Rd, NE MS-E05, Atlanta, GA 30333, USA. E-mail: RPerry{at}cdc.gov
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Abstract |
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Background Shortly after a measles supplementary immunization activity (SIA) targeting children from 9 months to 14 years of age that achieved high coverage, Burkina Faso had a large, serologically confirmed measles outbreak. To investigate the causes of this first reported failure of a widely successful measles control strategy we conducted a case–control study.
Methods Serologically confirmed measles cases aged 
9 months at the time of the SIA in 6 heavily affected districts were frequency matched on age to 3 controls recruited from people frequenting health centres in the same districts.
Results Between January and July 2002, 1287 measles cases were reported throughout Burkina Faso. Of the 707 cases that were serologically confirmed, 358 (51%) were from 9 months to 14 years of age and 265 (37%) were 15 years of age. Among cases and controls from 9 months to 14 years of age significant risk factors for measles were lack of measles vaccination and, in the unvaccinated, recent travel to Côte d'Ivoire. Of the recent measles cases in Côte d'Ivoire 54% were there when exposed to measles. Among adults, risk factors included non-vaccination and the lack of school attendance during childhood. Vaccine effectiveness was estimated to be 98%.
Conclusions Migration of children between Côte d'Ivoire and Burkina Faso played a major role in the failure of the SIA to interrupt measles transmission. Synchronization of measles control activities should be a high priority in countries with regions where much migration occurs.
Keywords Measles, migration, Burkina Faso, Côte d'Ivoire, outbreak investigation, retrospective study, surveillance, risk factors
Accepted 22 November 2004
Despite the existence of an inexpensive, safe, and highly effective vaccine, measles remains a major cause of childhood mortality and morbidity in many regions of the world. For the year 1999, the World Health Organization (WHO) estimated that measles contributed to 875 000 deaths worldwide, with more than half of these deaths occurring in Africa.1 To reduce this burden by 50% by 2005 the WHO has recommended a strategy that includes improving measles vaccination coverage together with providing a second opportunity for measles immunization to all children, either through a second routine dose or through periodic supplementary immunization activities (SIAs).2 These SIAs typically begin with a ‘catch-up’ SIA targeting children from 9 months to 14 years of age, followed by periodic ‘follow-up’ SIAs targeting children from 9 to 59 months of age.
Burkina Faso reflects the burden of measles in Africa with thousands of cases each year and regular epidemics as shown in Figure 1. The most recent large-scale measles epidemic in Burkina Faso was in 1996 with 43 123 reported cases followed by a smaller epidemic in 1999 with 12 157 reported cases.3 Measles control in Burkina Faso began in 1962 with mass vaccination activities targeting children from 6 months to 4 years of age, first through measles vaccine field trials and then through the Smallpox Elimination—Measles Control Program of the WHO.4,5 Mass vaccination activities were repeated in 1983 targeting children from 9 months to 6 years of age6 and in 19987 and 19998 targeting children from 9 to 59 months of age (Figure 1). Generally, the coverage of measles vaccination through routine services has been between 40 and 60% during the 1990s, with steady increases after 1999 to 64% in 2002.9
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In December 2001 a nationwide measles ‘catch-up’ SIA was held in Burkina Faso, targeting children from 9 months to 14 years of age. After the SIA, the Ministry of Health implemented the WHO regional guidelines for measles surveillance10 with individual reporting of cases and laboratory confirmation of all isolated cases and the first 5–10 cases of suspected outbreaks. A survey conducted after the SIA reported nationwide coverage of 97%.10 However, from January 1 to July 28, 2002, a total of 1287 suspected measles cases were reported in Burkina Faso. Measles was confirmed serologically in two-thirds of the reported cases with available results. Half of the confirmed cases were in age groups targeted by the SIA and one-third, were in older age groups. The majority of cases were reported during the typical measles epidemic season of January–June.4,6
This outbreak is the first reported failure of a strategy that has markedly reduced measles morbidity and nearly stopped measles mortality in the Americas4 and in seven Southern African countries.4 Understanding why this SIA apparently failed to interrupt measles transmission is critical to evaluating the use of wide age range SIAs and developing the most appropriate strategy for measles mortality reduction. In order to investigate the causes of this outbreak, we conducted a case–control study to identify risk factors for measles in children from 9 months to 14 years of age on December 15, 2001 and in people 15 years of age on that date.
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Methods |
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Measles surveillance
Since 1984, measles cases have been reported to the Ministry of Health through weekly aggregate district-level reporting. Case-based measles surveillance was introduced in 2000, with laboratory confirmation of a subset of suspected cases. After the December 2001 measles SIA laboratory confirmation of suspected cases was extended to include all reported cases nationwide. Cases are reported by staff at any health facility to the health district, from there to the provincial health authorities and from there to the Expanded Program on Immunization (EPI) at the Ministry of Health. For each suspected case, a blood sample is taken by venipuncture and a case investigation form is completed, recording age, sex, residence, date of onset, date of last vaccination, and vital status at the time of the report. Serological confirmation of measles is done at the Measles National Reference Laboratory in Ouagadougou at the Centre Hospitalier National Pédiatrique Charles de Gaulle using a commercially available IgM ELISA (Enzygnost, Dade-Behring, Marburg, Germany).
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Case–control study |
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Study site
The study took place in six health districts of Burkina Faso: Koudougou, Kongoussi, Saponé, Nanoro, Ouahigouya, and Yako. These districts were among those reporting the largest numbers of serologically confirmed cases. Also, the eligible cases in the selected districts were most evenly distributed between children from 9 months to 14 years of age and people
15 years of age.
Selection of cases and controls
Cases were individuals with serologically confirmed measles identified through the case-based measles surveillance system whose symptoms began between January 1 and July 29, 2002, were still living at the time of the case report and were 9 months of age on December 15, 2001 (the start date of the measles SIA). Cases were excluded if the predicted age on December 15, 2001 was <9 months or if they were unable to be located after three attempts.
For each measles case, three controls were recruited from people at health centres in the study districts. Controls were frequency matched to cases on age by selecting controls who fell in an interval centred on the case's age. Controls were ±6 months of the case's age for cases from 17 months to 3 years old, ±12 months for cases from 4 to 9 years old, ±2 years for cases from 10 to 14 years old, and ±5 years for cases 15 years old. Controls could be recruited from any health centre, with the number of controls recruited from each health centre proportional to the size of the centre's catchment population. Controls were excluded if they were <9 months of age on December 15, 2001 or if they had a history of measles between January 1 and July 29, 2002.
During household visits, written informed consent to participate in the investigation was requested from adult participants and from parents/guardians of children <15 years of age. Only those giving consent were interviewed.
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Data collection |
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Information on potential risk factors was collected through a questionnaire. The interviews were conducted in Moré, the local language, between August 25 and October 10, 2002 by trained interviewers normally working outside the health sector. Travel history was sought by questions asking for location of usual residence, frequency and destination of trips outside the district, where the interviewee was at the time of the SIA and, for cases, their location during the periods of rash and of potential exposure to measles. Vaccination status was assessed by both card and recall with routine and SIA doses asked about separately. During the SIA, the supply of vaccination cards was delayed and so not all vaccinated children received a card.
Data analysis
Data from questionnaires were entered into a computerized database using EpiInfo 6.04d (Centres for Disease Control and Prevention and World Health Organization, Atlanta, GA). Analysis was done using SAS version 8.2 (SAS Institute, Cary, NC). Cases and controls from 9 months to 14 years of age on December 15, 2001 were analysed separately from cases and controls 15 years of age on that date. Recent travel or migration was defined as that occurring within the 12-month period before the date of the interview. To compensate for missing information on education or occupation of the parents, variables were constructed taking the father's information, if available, and if not, the mother's information. Multiple logistic regression was used to calculate age-adjusted odds ratio and multiply adjusted odds ratios (ORs) and 95% confidence intervals (CIs) for measles. Age adjustment was done by including indicator variables for age group, omitting the variable for the referent group. Vaccine effectiveness (VE) was estimated using the following formula: VE = 1 2 OR.14 The Cochran–Mantel–Haenszel (CMH) test was used to test the association between travel and measles in unvaccinated children aged from 9 months to 14 years.
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Results |
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TopAbstractMethodsCase-control studyData collectionResultsDiscussionReferences |
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Measles surveillance
Based on the date of rash onset of reported cases, measles cases began to increase in number after the SIA in January 2002, were highest in March (271 cases), April (424 cases), and May (315 cases) and were fewer after mid-July. Serum specimens were collected from 1044 (81%) of the 1287 individually reported cases, with results available for 1024 (80%) and positive results in 707 (55% of all individually reported cases and 69% of those tested). Of the confirmed cases 358 (51%) were in the age group targeted by the SIA and 15% of confirmed cases in the target age group had a history of vaccination (Figure 2). A high proportion of confirmed cases, 37%, were people >15 years of age. Of the confirmed cases 51% were male. Cases were reported from 48 (91%) of 53 health districts though the majority of cases were from the north-central part of the country (Figure 3).
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Case–control study
Health authorities in the six districts chosen for the case–control study received individual reports of 494 suspected measles cases. Of the 358 cases 263 (73%) with available samples were serologically confirmed and after excluding those <9 months of age on December 15, 2001 or with a history of measles during 2002, 186 (52%) of the 358 were eligible for the study. Of the 186 eligible cases and the corresponding 558 controls, the field teams were able to recruit 134 cases and 556 controls (Table 1). Of those cases between 9 months and 14 years of age, 69 of 97 (71%) were found, compared with 65 of 89 (73%) cases
15 years of age. The most common reason a case could not be enrolled was that the individual had moved away from the study area. Of the 37 who left 30 people had gone to Côte d'Ivoire, with 21 (70%) of those going to Côte d'Ivoire being from 9 months to 14 years of age.
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The distribution of cases was roughly equal between the six districts, while the distribution of controls was proportional to the district population (Figure 3). For both age groups, cases and controls were similar with respect to age, gender, and ethnicity (Tables 2 and 3), though the median age of cases was slightly older than that of controls for those from 9 months to 14 years of age. A history of measles was found for 17 (6%) of 292 controls aged from 9 months to 14 years and for 61 (23%) of 262 adult controls. Repeating the analysis with these controls excluded does not change the factors significantly associated with the risk of measles in the bivariate or multivariate analyses presented here.
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Cases and controls aged from 9 months to 14 years
In children aged from 9 months to 14 years, measles cases were more likely than controls to live
5 km from a health centre, to never have attended school, to be from a rural zone, to live in a household with 15 people and to have a parent who worked as a farmer, or who never attended school (Table 2). Cases were also more likely to have recently travelled outside their district of residence, especially to Côte d'Ivoire, and to lack a history of measles vaccination. Vaccination status interacted significantly with recent travel (Table 4). Among unvaccinated cases and controls, recent travel outside the district was a risk factor for measles, with an age-adjusted OR of 8.64 (CI 1.44–51.8) while for vaccinated cases and controls, travel outside the district was not a risk factor, with an age-adjusted OR of 0.82 (CI 0.27–2.51). Large household size also interacted with vaccination status, with an age-adjusted OR of 11.4 (CI 2.60–49.6) in vaccinated cases and controls and 0.68 (CI 0.15–3.20) in the unvaccinated.
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In the multivariate model, the significant risk factors for measles were non-vaccination, living far from a health centre, large household size, and recent travel (Table 5). Non-vaccination significantly interacted with both household size and recent travel: large household size was a risk factor only in the vaccinated, while recent travel was a risk factor only in the unvaccinated. Though the educational status of the child and the educational and occupational status of the parents were not significant risk factors in the multivariate model, exclusion of these factors changed the ORs for vaccination and travel enough to suggest they were important confounders and so were left in the model.
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Much of the risk from recent travel outside the district came from recent travel to Côte d'Ivoire. Whereas 26 (84%) of the 31 cases travelling outside the district had gone to Côte d'Ivoire, only 10 (18%) of the 55 controls travelling outside the district had gone to Côte d'Ivoire. Travel to Côte d'Ivoire also interacted with vaccination, with recent travel to Côte d'Ivoire being a strong risk factor in unvaccinated (age-adjusted CMH 9.26, P = 0.0023) but not in vaccinated children (age-adjusted CMH 1.43, P = 0.23). All 24 unvaccinated cases with a history of recent travel to Côte d'Ivoire were there in December 2001 during the time of the measles SIA in Burkina Faso. Travel to Côte d'Ivoire was also associated with exposure to measles. When asked where they were during the exposure period 7–21 days before rash onset, 14 cases reported being in Côte d'Ivoire, one with a history of vaccination and 13 without. This number represents 21% of all cases and 54% of the 26 cases with a history of travel to Côte d'Ivoire.
Cases and controls aged 15 years
In adults 15 years of age, in both the bivariate and multivariate analyses, measles cases were more likely than controls to live 5 km from a health centre, never to have attended school and lacking a history of vaccination (Tables 5 and 6). The parents of cases in adults were more likely to have worked as farmers, though this variable was not included in the multivariate model as data were available for only two-third of cases and controls. The number of people living in the household, the history of education in the parent, and recent travel were not significant risk factors in this age group. When asked where they were 7–21 days before rash onset, only 5% (3/65) cases reported being in Côte d'Ivoire.
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Vaccine effectiveness and SIA coverage
The effectiveness of vaccine given during the SIA was estimated in the 42 cases and 34 controls whose only dose of measles vaccine was the one given during the SIA. The age-adjusted OR for measles vaccination in these children was 0.01 (95% CI 0.002–0.08), giving an estimated vaccine effectiveness of 99% (95% CI 92–100%). In the six health districts studied, 87% of the controls aged from 9 months to 14 years reported having been vaccinated during the SIA, as compared with the nationwide SIA coverage of 97% (95% CI 94–99%) obtained through a cluster survey done 1 month after the SIA.
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Discussion |
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TopAbstractMethodsCase-control studyData collectionResultsDiscussionReferences |
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In 2002 Burkina Faso experienced a nationwide measles outbreak soon after a measles SIA that achieved high coverage. The case-based surveillance data suggest that large pockets of unvaccinated children existed despite the SIA and many adults had escaped previous exposure to measles despite regular epidemics in Burkina Faso with thousands of reported cases. The case–control study found that in adults a key factor in this outbreak was the lack of school attendance during childhood. According to the 1998 demographic and health survey, rates of school attendance in Burkina Faso are low, with roughly 30% of adults having ever attended school.15 Adults who never went to school could remain susceptible to measles for many reasons, for example lack of exposure to classmates with measles. Many measles outbreaks have been reported in schools, in both USA16 and Africa.17,18
Clearly, lack of vaccination was the main risk factor found in this study. Another important factor in this outbreak was the movement of unvaccinated children into Burkina Faso from Côte d'Ivoire, many already incubating measles. In addition to the 26 children found with a history of recent travel to Côte d'Ivoire, 21 of the 28 children with confirmed measles but not found had also gone to Côte d'Ivoire. Overall, 55% (52/95) cases in this age group were linked to travel to Côte d'Ivoire. Though this study was not designed to identify risk factors for non-vaccination, 50% (24/48) of the children with a history of recent travel were unvaccinated, compared with 4% (12/286) who had not travelled. In adults, cases were more likely to have been in Burkina Faso during the exposure period and travel was not a risk factor, suggesting that this outbreak arose from the importation of measles into Burkina Faso from Côte d'Ivoire, together with many unvaccinated children, resulting in an outbreak that spread to susceptible children and adults already residing in the country.
Migration from Burkina Faso to Côte d'Ivoire was encouraged during 1950s–1980s to supply labour for Ivorian agricultural plantations and construction sites.19,20 Migrants were at first single male labourers and later entire families who would move back and forth between the two countries.19,20 As a result, in 1998 more than 2.2 million Burkinabé were estimated to be living in Cote d'Ivoire,21 compared with a total population of Burkina Faso of 11 million.22 Over the past few years people have been returning as a result of the economic and political problems in Côte d'Ivoire, with over 340 000 returning in the 12 months after the attempted coup in September 2002.23 Returning children are not likely to be vaccinated, as Côte d'Ivoire has not held a nationwide measles SIA and reports low routine measles vaccination coverage (56% in 200224), and to be exposed to measles, as the yearly number of reported measles cases since 1996 in Côte d'Ivoire has ranged from 4824 to 20 858, with 7633 reported cases in 2002.25
Population movements have affected the distribution of disease throughout history.26 While the most striking examples are when migrants introduce diseases into new areas, such as measles in the Americas and the South Pacific,27 population movements also cause the re-importation of diseases into regions where they have been brought under control, as has been seen with measles,28–30 tuberculosis,31,32 malaria,33 rubella,34,35 lymphatic filariasis,36,37 and polio.38–40 Population movements bringing together large numbers of unvaccinated or otherwise susceptible people can also lead to disease outbreaks. The immigration of susceptible people from Mexico has resulted in rubella outbreaks in the USA35,41 and in Sao Paulo, Brazil a large measles outbreak was associated with the migration of unvaccinated young adults from more rural areas.42
The results of this study also suggest that the coverage achieved by the SIA was in fact lower than that estimated by the post-SIA coverage survey. This difference may in part be the result of the influx of unvaccinated children from Côte d'Ivoire that occurred in the months between the SIA and the study. In addition, the controls are not a representative sample of children <15 years of age, as they were recruited from people frequenting health centres, and came from districts selected because they had the highest number of reported cases. The study data do not suggest that vaccine failure played a major role in this outbreak.
A limitation of this study was that we could only enrol 38% of all suspected cases of measles reported from the study districts. Much of this reduction was because of the requirement for laboratory confirmation of measles. Relying on laboratory-confirmed cases reduced misclassification of disease status, but may have made the study population less representative of all cases. The risk factors for measles found in this study may not be the same as those in other districts of Burkina Faso. However, a significant proportion of all reported and lab-confirmed cases came from the study districts. These districts were also similar to non-study districts in terms of the proportion of cases that were laboratory confirmed, the proportion in the age group targeted by the SIA and the proportion with a history of measles vaccination. The controls in this study were recruited from people seeking health care at health centres throughout the study districts, and not just the areas where the cases originated. Thus, the controls may not have had the same opportunity for exposure to measles as the cases. However, the cases themselves were only those people with measles who sought health care at health centres in the study area. The method used selects controls in the same manner, from those seeking health care, and reduces over-matching on factors related to location, such as vaccination coverage, school attendance, and travel history.
The results of this study suggest that migration played a large role in the failure of the measles SIA to interrupt measles transmission in Burkina Faso. These results also show the importance of timely, data-driven outbreak investigations to identify the true causes of an outbreak. Achieving sustainable reductions in measles morbidity and mortality in Burkina Faso will remain difficult without simultaneously improving measles control in Côte d'Ivoire. Based on the results of this investigation, the WHO, UNICEF, and other members of the Measles Initiative43 are planning synchronized, multi-country SIAs throughout West Africa, including a ‘catch-up’ SIA in Côte d'Ivoire and a ‘follow-up’ SIA in Burkina Faso. Such synchronized SIAs should be done in other regions where much migration occurs, similar to what has been done for polio eradication.44
These results highlight the need to identify population movements and anticipate their effects when planning disease control programs, particularly for highly infectious diseases such as measles. International public health agencies, such as those forming the Measles Initiative, can play an important role in tracking changing migration patterns and in facilitating disease control efforts co-ordinated between countries. Individual countries also should ensure that all people on their territory, even if undocumented, fully benefit from public health interventions such as vaccination. Ignoring population movements is detrimental to a disease control program, may be because of the loss of public trust when the program ‘fails’ or because of the costs of repeating the program interventions after adapting them to population movements.
KEY MESSAGES
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Acknowledgments |
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Funding for this investigation was provided by the World Health Organization and the Ministry of Health, Burkina Faso. We wish to thank the following people for their support throughout the duration of the study: Dr Mohamed-Mahmoud Hacen, the WHO Representative to Burkina Faso, the late Colonel Dr Clément Zidouemba, head of the Direction de la Médecine Préventive of the Ministry of Health of Burkina Faso, Dr Katimou Maga, Dr Patrick Zuber, Dr Margarette Kolczak, and the many others who helped with the data collection and analysis.
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Notes |
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The results of this study were presented in part at the Third Annual Meeting of Partners for Measles Advocacy in Washington, DC, in February 2003. 
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References |
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