BCG coverage and barriers to BCG vaccination in Guinea-Bissau: an observational study
© Thysen et al.; licensee BioMed Central Ltd. 2014
Received: 23 May 2014
Accepted: 29 September 2014
Published: 4 October 2014
BCG vaccination is recommended at birth in low-income countries, but vaccination is often delayed. Often 20-dose vials of BCG are not opened unless at least ten children are present for vaccination (“restricted vial-opening policy”). BCG coverage is usually reported as 12-month coverage, not disclosing the delay in vaccination. Several studies show that BCG at birth lowers neonatal mortality. We assessed BCG coverage at different ages and explored reasons for delay in BCG vaccination in rural Guinea-Bissau.
Bandim Health Project (BHP) runs a health and demographic surveillance system covering women and their children in 182 randomly selected village clusters in rural Guinea-Bissau. BCG coverage was assessed for children born in 2010, when the restricted vial-opening policy was universally implemented, and in 2012–2013, where BHP provided BCG to all children at monthly visits in selected intervention regions. Factors associated with delayed BCG vaccination were evaluated using logistic regression models. Coverage between intervention and control regions were evaluated in log-binomial regression models providing prevalence ratios.
Among 3951 children born in 2010, vaccination status was assessed for 84%. BCG coverage by 1 week of age was 11%, 38% by 1 month, and 92% by 12 months. If BCG had been given at first contact with the health system, 1-week coverage would have been 35% and 1-month coverage 54%. When monthly visits were introduced in intervention regions, 1-month coverage was higher in intervention regions (88%) than in control regions (51%), the prevalence ratio being 1.74 (1.53-2.00). Several factors, including socioeconomic factors, were associated with delayed BCG vaccination in the 2010-birth cohort. When BCG was available at monthly visits these factors were no longer associated with delayed BCG vaccination, only region of residence was associated with delayed BCG vaccination.
BCG coverage during the first months of life is low in Guinea-Bissau. Providing BCG at monthly vaccination visits removes the risk factors associated with delayed BCG vaccination.
KeywordsBCG Coverage Timeliness of vaccines Implementation of the vaccination programme
Bacillus Calmette Guérin (BCG) vaccine is recommended at birth to normal-birth-weight children in Guinea-Bissau. However, BCG vaccination is often delayed for several reasons, one of them being the “restrictive vial-opening policy”: BCG is a freeze-dried vaccine supplied in vials with 20 infant doses  and once reconstituted, the vaccine should only be used for a maximum of six hours. In Guinea-Bissau and other low-income countries [2, 3], the focus on not wasting vaccines  has led to a policy of not opening a BCG vial unless 10 children are present to be vaccinated . Previous studies have shown that BCG has beneficial non-specific or heterologous effects, providing protection also against many non-tuberculosis causes of death [6–15]. In two randomised trials among low-birth-weight (<2500 g, LBW) neonates, BCG at birth compared with the usual delayed BCG, lowered neonatal mortality by 48% (95% CI: 18%-67%) [6, 7], the reduction being 58% (8%-81%) the first three days after vaccination [6, 7]. The rapidly occurring effect suggests that BCG stimulates the innate immune system. This is supported by recent immunological studies showing that BCG induces epigenetic changes which reprogram monocytes to increased pro-inflammatory responses against unrelated pathogens [16, 17].
Most infant deaths occur during the neonatal period, particularly in the first week of life  and thus any delays in BCG vaccination may have major consequences because children do not benefit from BCG when their mortality risk is highest. Hence, it is important to identify obstacles to early BCG vaccination, as this will help target interventions to lower the age at vaccination.
We assessed BCG coverage at different ages among children born in 2010 in rural Guinea-Bissau to identify factors associated with delayed BCG vaccination in a context with a restrictive vial-opening policy. In 2012, we implemented monthly visits and provided BCG vaccination to newborns in three intervention regions (Oio, Biombo and Cacheu) but not in six control regions. We evaluated how not adhering to the restrictive vial-opening policy affected BCG coverage and affected factors associated with delayed BCG vaccination.
Setting and study population
The study was conducted in the rural study area of the Bandim Health Project (BHP) in Guinea-Bissau. The BHP maintains a health and demographic surveillance system following 182 randomly selected clusters of 100 women and their children in rural Guinea-Bissau. The clusters were initially selected using the Expanded Programme on Immunizations (EPI) methodology for immunisation surveys sampling 20 clusters of 100 women in each of the eight larger health regions, and 10 and 12 clusters in the two smallest regions. Later two regions have been joined and rural Guinea-Bissau now has nine health regions; Oio, Biombo, Gabu, Cacheu, Bafata, Quinara, Tombali, Bubaque, and Bolama. All women of fertile age and children below the age of 5 years are followed through home visits every four to six months.
At the home visits women of fertile age are registered and information on ethnicity and schooling is collected. If a pregnancy is registered, a special form is completed collecting information on prenatal consultations and socioeconomic factors. For all newborn children information on date of birth, place of birth, and prenatal consultations is collected. At all visits the child’s vaccination card is inspected and vaccination dates are recorded. If the child has no vaccination card a vaccination card is provided from the BHP team.
BCG vaccination possibilities
Children in Guinea-Bissau should receive BCG and oral polio vaccine (OPV) at birth, pentavalent vaccine (diphtheria-tetanus-pertussis-H. influenza type B-Hepatitis B vaccine) and OPV at 6, 10, and 14 weeks, and measles and yellow fever vaccines at 9 months. These vaccines are provided free of charge at the health centres as part of the national programme and during outreach to villages when additional funding is available. Due to the restricted vial-opening policy some vaccines are only provided once a week at health centres and only if there is a sufficient number of eligible children present.
Since 2007 the BHP teams visiting the surveyed villages in all regions have been accompanied by a nurse, who offered OPV, pentavalent vaccine, measles vaccine, and yellow fever vaccine to all children below the age of 1 year. The vaccines were supplied through the national programme and the BHP nurse had to follow the national policy. Hence she did not bring BCG as she would very rarely encounter sufficient eligible children in a village.
In 2012 the BHP increased the frequency of visits from four-six-monthly visits to monthly visits in three regions (Oio, Biombo and Cacheu). In these intervention regions BCG vaccination was offered to all children below the age of 1 year regardless of the number of children present, thus a BCG vial was opened for one child. In the remaining control regions national policy was followed and BCG was not offered during village visits.
Information about reasons for delay of BCG vaccination
During the year from 1st July 2012 to 30th June 2013 mothers of BCG unvaccinated infants in all regions were interviewed on their BCG vaccination attempts/experiences during home visits. They were asked if they knew that their child was due to receive BCG and whether they had taken the child for vaccination. Mothers who reported to have sought vaccination were asked why the child had not been vaccinated. Mothers who had not sought BCG vaccination were interviewed about the reasons.
BHP’s HDSS which has been in place in Guinea-Bissau since 1978 and is conducted by request from the Guinean Ministry of Health. The current surveillance system in the rural areas has been approved by the National Ethics Committee in Guinea-Bissau and the Central Ethics Committee in Denmark. No separate ethical and consent approval was sought.
Assessing BCG coverage in the 2010-birth cohort
Coverage assessment methods for standard coverage estimates and coverage estimates in the 2010-birth cohort and the 2012 cohort
Standard coverage estimates
Coverage in 2010-birth cohort
Coverage in 2012 cohort
Children born in 2010
Children aged 1, 3, 6, or 12 months of age, when visited from 1st July 2012 to 30th June 2013
1 week, 1, 3, 6 and 12 months
1, 3, 6, and 12 months
First visit with seen vaccination card within 12 months after assessment age
Visit with seen vaccination card in the month after the assessment age
Missed opportunities among BCG unvaccinated children were defined as contact with the health system, either being born at a health facility or having received other vaccines (based on the registered date of another vaccination on the vaccination card). We calculated the potential coverage if BCG had been given at the first contact with the health system.
Assessing BCG coverage after implementation of monthly visits, 2012 cohort
In 2012 monthly visits were introduced in the intervention regions, whereas four-six-monthly visits continued in control regions. We considered a village as belonging to the intervention regions when there was less than 6 weeks between two subsequent visits. BCG coverage was assessed among all children visited from 1st July 2012 to 30th June 2013. Like in the 2010-birth cohort, we assessed BCG coverage at 1, 3, 6, and 12 months of age. To take into account that children in intervention regions with monthly visits had a larger possibility of having their card seen within a 12 months period compared with children in control regions with four-six-monthly visits, we considered only data collected in the month after 1, 3, 6, and 12 months, respectively (Table 1).
Comparisons of coverage between regions with different BCG provision strategies were evaluated in log-binomial regression models providing prevalence ratios (PR).
Factors associated with delayed BCG vaccination
Factors associated with delayed BCG vaccination (vaccination after 1 month of age) were assessed in the 2010-birth cohort and after implementation of monthly visits separately for intervention and control regions in 2012/2013. This study focused on background factors assessed among the users of the vaccination services. The factors evaluated were: sex, birth place, antenatal care, region, type of roof, toilet, household possessions (radio, cell phone, and generator), ethnic group (Fula, Pepel, Balanta, Manjaco, and other), age of mother, and education of caretaker. All continuous variables were tested for linear relationship with BCG coverage by inspecting the BCG coverage in quintiles of the variable. Where inspection suggested a linear relationship, the quadratic value of the continuous variable was included in the model to assess departure from linearity. We tested all variables one by one in a simple model using logistic regression to calculate the odds ratio (OR) of being unvaccinated. As children were not individually sampled but selected for the study based on residence within a geographical cluster, we adjusted the standard error for cluster. In a larger multivariable model we included all factors associated with delayed BCG. In this large model we excluded ethnic group since ethnic group and region were highly correlated with more than 90% of the Pepels living in Biombo, and more than 75% of the Manjacos living in Cacheu. We chose to include region rather than ethnicity since region would be feasible to target through interventions.
BCG coverage in the 2010-birth cohort
BCG coverage after implementation of monthly visits, 2012 cohort
Factors associated with delayed BCG vaccination in the 2010-birth cohort
Factors associated with BCG vaccination by 1 month of age
Total number of children
BCG by 1 month n (%)
OR of BCG vaccination1
Multivariable analysis OR (95%CI)1
P-value for the univariate/multivariable analyses
Age of mother 2
2. quartile (21–24)
3. quartile (25–30)
4. quartile (>30)
Education of caretaker 3,4
Ethnic group 6
Contact with the health system
Birth place 7
Prenatal consultations 8
Type of roof 9
Latrine/ toilet in house
Cell phone 11
The risk factor analysis for BCG coverage by 3, 6, and 12 months identified the same factors but most associations were weaker. Prenatal consultation was significantly associated with BCG coverage at all ages (data not shown).
Factors associated with delayed BCG vaccination after implementation of monthly visits, 2012 cohort
Factors associated with BCG vaccination by 1 month of age after implementation of monthly visits in intervention regions
BCG by 1 month n (%)
OR of early BCG vaccination1
Multivariable analysis OR (95% CI)1
P-value for the univariate/multivariable analyses
BCG by 1 month n (%)
OR of early BCG vaccination1
Multivariable analysis OR (95% CI)1
P-value for the univariate/multivariable analyses
0.492 / 0.662
Age of mother 3
0.582 / 0.615
2. quartile (21–26)
3. quartile (27–31)
4. quartile (>31)
Education of caretaker 4, 5
0.003 / 0.377
<0.001 / 0.002
Ethnic group 7
0.109 / NA
Contact with the health system
Birth place 8
0.369 / 0.515
Prenatal consultations 9
0.410 / 0.504
Type of roof 10
0.048 / 0.128
0.039 / 0.188
Latrine/ toilet in house
Cell phone 12
0.011 / 0.136
0.183 / 0.303
0.020 / 0.083
Information about reasons for not being BCG vaccinated
The year following implementation of monthly visits in intervention regions, 1470 interviews were conducted with mothers of BCG unvaccinated children from all regions. Among the mothers 229 (16%) reported to have sought vaccination for their child, 135 (59%) recalled to be told to return another day to get the vaccine, and 76 (33%) had received other vaccines (Additional file 3). Among the 1239 mothers, who reported not to have sought vaccination, 760 (61%) reported that their main reason was lack of money whereas 481 (39%) said that the distance to the vaccination post kept them from seeking vaccination (Additional file 3).
In 2010, BCG coverage by 1 week of age was only 11% in rural Guinea-Bissau. By 1 month of age the coverage was 38%, increasing to 73% by 3 months of age and 92% by 12 months of age. Contact with the health system was one of the main factors associated with BCG vaccination, but socioeconomic factors also played a role. When monthly visits were introduced in intervention regions and BCG was available for all children the inequity was reduced and the 1-month BCG coverage was 88% compared with 51% in control regions.
Strengths and weaknesses
A major strength of this study is the set-up in the form of the health and demographic surveillance system covering a representative part of the population in rural Guinea-Bissau. Data was collected through frequent home visits by experienced field workers. Weaknesses include that children who died before the assessment age did not enter the coverage analysis; however, children dying before 12 months of age usually do not enter the standard coverage estimation either. Also it should be noted that the vaccination coverage was estimated using slightly different approaches in the 2010-birth cohort and the 2012 cohort. However, we do not directly compare coverage between the cohorts, but only compare coverage between intervention and control regions within the 2012 cohort. Information on reasons for not being vaccinated was collected based on the mothers’ recall.
Consistency with other studies
Vaccination coverage is usually reported by 12 months of age. We found 92% BCG coverage by 12 months in 2010, which corroborates the 94% coverage from 2009 reported by WHO . Others have found that the median vaccination coverage across 31 low- and middle-income countries was 98% and ranged from 56% to 100% .
We found a much lower coverage by 1 and 3 months, which concurs with reports of a median coverage across the 31 countries of 65% by age of 4.3 weeks, ranging from 15% to 97% . This supports the need for assessing BCG coverage at earlier ages to disclose the delay in BCG vaccination.
Other studies [22–24] defined timely BCG vaccination as vaccinated before 8 weeks of age. The percentage of timely vaccinated children ranged from 69% vaccinated  in a large survey in 45 low-income and middle-income countries, to 99%  in a study from three areas in South Africa. This still does not fully disclose the poor coverage in the neonatal period, with only 49% coverage by 4 weeks , quite similar to the 1-month coverage of 38% in the present study.
We found that giving birth at a hospital or health centre increased the likelihood of being BCG vaccinated. Similarly, a study from South Africa found that birth at a health facility reduced the risk of being unvaccinated by 47% (26%-42%) . In Ethiopia there was also higher BCG coverage for those born at a health facility . In Guinea-Bissau it is not general practice that children born at a hospital or health centre are vaccinated before they leave the health facility, however, they are often told to return to the health centre for vaccination.
It has previously been reported from South Africa  and 31 low- and middle-income countries  that low socioeconomic status was related to delay in BCG vaccination. We found a similar tendency, especially during the first month of life. Importantly, this inequity in getting BCG vaccinated was no longer apparent when we provided BCG at monthly village visits.
Interpretation and implications
WHO vaccination coverage estimates are reported as the coverage by 12 months of age not taking into account the timeliness of vaccines received. This does not disclose delays in administration of the BCG vaccine. It has been shown that BCG vaccination can reduce neonatal mortality by 48% in LBW children when administered at birth . When donors only ask for BCG coverage by 12 months of age, there is no incentive to provide BCG in the neonatal period. Therefore the 1-month coverage or the median age at vaccination would be better indicators of BCG coverage and its likely effect on child survival.
Obstacles to timely BCG were identified through the interview with mothers of unvaccinated children. Among the mothers having sought vaccination but had not obtained BCG more than half the mothers recalled being told to return another day. We speculate that the restricted vial-opening policy is one of the main obstacles to early BCG vaccination but the information disclosed to the mothers does not allow any final conclusion. Among the mothers who had not sought vaccination not having money and distance to health facility were the main obstacles to taking their child for vaccination. Routine childhood vaccinations are provided free of charge in Guinea-Bissau, but health workers charge fees (~1$) for vaccination cards.
Twenty-five percent of BCG unvaccinated children had been in contact with a health facility by 1 month of age. The potential coverage by 1 month of age was 54% in 2010, if all children had been BCG vaccinated at first contact with the health system. Monthly village visits with BCG vaccination for all children significantly increased BCG vaccination coverage, especially at early ages, and would provide a very efficient tool for increasing especially coverage among the youngest children.
Our study showed a large delay in BCG vaccination in Guinea-Bissau with less than half of the children being BCG vaccinated by 1 month and only 11% being BCG vaccinated by 1 week of age. Our risk factor analysis identified many factors associated with delay of BCG vaccination, including a number of socioeconomic factors, but these factors were no longer associated with delayed BCG vaccination when BCG-vaccination became available to all children at monthly visits.
Bacillus Calmette-Guérin vaccine
Bandim Health Project
Oral polio vaccine
World Health Organization.
Funding: The study was funded by Aarhus University, Aase og Ejnar Danielsens Fond, Dagmar Marshalls Fond, Direktør Michael Hermann Nielsens Fond, Fonden til lægevidenskabens fremme and European Union FP7 support for OPTIMUNISE (grant: Health-F3-2011-261375). The Bandim Health Project received support from Danish National Research Foundation via support to CVIVA (grant: DNRF108). PA holds a research professorship grant from the Novo Nordisk Foundation, CSB an ERC stating grant (grant: ERC-2009-StG-243149 and ABF a postdoc grant from the Danish Council for Independent Research (DFF – 1333–00192). The funding agencies had no role in the study design, in the data collection, analysis, and interpretation, or in the writing of the report.
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