Low vaccine coverage among children born to HIV infected women in Niamey, Niger

Abstract

Background: The effect of mother’s HIV-status on child vaccination is an important public health issue in countries with high HIV prevalence. We conducted a study in a primary healthcare center located in Niamey, the capital of Niger, which offers free of charge services to HIV positive and/or underprivileged mothers, with the aim of assessing: 1) vaccination coverage for children 0–36 months old, born to HIV-infected mothers, and 2) the impact of maternal HIV status on child vaccination. Methods: Mothers of children less than 36 months old attending the center were interviewed, to collect information on vaccines administered to their child, and family’s socio-demographic characteristics. Results: Overall, 502 children were investigated. Children of HIV-seropositive mothers were less likely to receive follow up vaccinations for Diphtheria-Tetanus-Pertussis (DTP) than those of HIV-seronegative mothers, with a prevalence ratio (PR) of 2.03 (95%CI: 1.58–2.61). Children born to HIV-seropositive mothers were less likely to miss vaccination for MMR than those born to HIV negative mothers, with a RR of 0.46 (95%CI: 0.30–0.72). Conclusions: Vaccine coverage among children born to HIV infected mothers was rather low. It is important to favor access to vaccination programs in this population.

Keywords:

• children
• HIV
• measles
• niger
• niamey
• vaccination

Abbreviations

DTP	=	Diphtheria-Tetanus-Pertussis
NGO	=	Non-Governmental Organization
BCG	=	Bacille Calmette Guerin
OPV	=	oral polio
HB	=	hepatitis B
Hib	=	haemophilus influenzae type B
MMR	=	Measles Mumps Rubella
WHO	=	World Health Organization
OR	=	Odds ratio.

Background

Over two million deaths are avoided through immunization programs each year worldwide.¹ Nevertheless, child vaccination coverage, especially in developing countries, is still far from international standards, leading to preventable morbidity and mortality.^2,3 Several factors, such as maternal age, maternal education, distance to health care facilities, household wealth,^4,5 maternal HIV serostatus,⁶ availability of safe needles and syringes are associated with missed or incomplete childhood vaccination.

Few studies investigated factors influencing immunization decisions among underprivileged women which live in urban area. These include poverty, ethnicity, place of delivery, mother’s education and parity of the mother.⁷ Whether maternal HIV status may influence parental adherence to vaccination schedules in this population group is still undefined. Perhaps, effects of maternal HIV status on vaccination coverage may be intensified for this population group compared to others, because of their low health status, the lack/poor quality of basic health services and antenatal care offered to them and their socio-cultural (e.g. gender related) and economic circumstances.

The relationship between mother’s HIV status and child vaccination is especially important in this context because of the heightened HIV prevalence.⁸ Actually, the risk of mortality increases for children born to HIV-positive mothers irrespective of their own HIV status,⁹ and it may not be excluded that this is in part due to the fact that they are less likely to receive routine childhood vaccinations. HIV positive mothers may be too sick or too poor to bring their children to vaccination clinics,¹⁰ or they may be reluctant to access primary health care clinics for fear of stigma. HIV infection may be also an indicator of risk taking behavior, and mothers who are more tolerant about risks to their own health might be less motivated to ensure their children receive risk-reducing interventions, such as vaccinations.⁶

We conducted a study in a primary healthcare center in Niamey, the capital of Niger which offered free of charge services to HIV positive and/or under-privileged mothers, with the aim of assessing: 1) vaccination coverage for children 0–36 months old born to HIV-infected mothers and 2) the impact of maternal HIV status on child vaccination.

Results

The characteristics of the children whose mothers were enrolled in the study are reported in Table 1. Overall, 502 children (262 female and 240 male) were investigated, including 257 HIV-seropositive children; the median age was 6 months for HIV-negative (range 0 d to 36 months) and 5 months for HIV-positive children (0 d to 24 months).

Table 1. Characteristics of the children by HIV status

	HIV- (N = 245)		HIV+(N = 257)		Total
	N	(%)	N	(%)	N	(%)
male sex	99	(40)	141	(55)	240/502	(48)
median age, mm	6	(0–36)	5	(0–24)	6	(0–36)
median weight, kg	6	(1–15)	6	(1–13)	6	(1–15)
breastfeeding	223	(91)	250	(97)	473/485	(97)
high SEP	23	(9)	40	(15)	63/486	(13)
DTP dose 1	225	(92)	241	(94)	466/502	(93)
DTP dose 2	107/209	(51)	16/209	(8)	123/418	(29)
DTP dose 3	69/138	(50)	8/119	(7)	77/257	(30)
MMR	23/74	(31)	32/48	(67)	55/122	(45)
BCG	241	(98)	257	(100)	498/ 502	(99)

SEP: socio-economic-position; DTP: diphtheria, tetanus and pertussis; BCG: Bacille Calmette Guerin; MMR: Measles, Mumps, Rubella.

Overall, 93% of the children received the first dose of DTP vaccine, 29% the second, and 30% the third dose. Children born to HIV-positive and HIV-negative mothers were equally likely having received the first dose of vaccine, while those born to HIV-positive mothers were less likely to have received the second and third those of DTP than their counterparts born to HIV-negative mothers (see Tables 1 and 2).

Table 2. Characteristics of the children by vaccination status for DTP

	Partially vaccinated		Fully vaccinated
	N = 332	(%)	N = 170	(%)	p
male sex, %	163	(49)	77	(45)	0.451
median age, mm	6	(0–36)	5	(1–36)	0.996^a
median weight, kg	6	(1–140)	6	(2–15)	0.212
breastfeed, %	321	(96)	152	(89)	0.218
median time breastfeed, mm	4	(0–24)	2	(0–36)	0.537
high SEP, %	37	(11)	26	(15)	0.115
median age at mandatory vaccination, mm	0	(0–14)	0	(0–7)	0.232
mothers HIV+, %^b	207	(62)	50	(29)	<0.001^b

^a Medians were tested with the Wilcoxon rank-sum test;

^b PR adjusted in a log-binomial regression using age and social class as categorical variables = 2.03 (1.58-2.61) p < 0.001.

Almost all the children included in the study received BCG vaccination within the first week after birth. About 67% of children of 9 months of age or older, born to HIV positive mothers, received MMR compared to the 31% of those born to HIV negative mothers (see Table 3).

Table 3. Characteristics of the children by vaccination status for MMR

	Not vaccinated		Vaccinated
	N = 439	(%)	N = 62	(%)	p
male sex, %	33	(8)	31	(50)	0.584
median age, mm	12	(9–24)	14	(9–36)	0.111^a
median weight, kg	9	(3–15)	9	(7–13)	0.505
breastfeed, %	51	(12)	54	(87)	0.363
median time breastfeed, mm	9	(2–24)	11	(1–36)	0.191
high SEP, %	14	(3)	3	(5)	0.008
median age at mandatory vaccination, mm	1	(0–12)	1	(0–3)	0.232
mothers HIV+, %^b	15	(3)	32	(52)	<0.001^b

^a Medians were tested with the Wilcoxon rank-sum test;

^b PR adjusted for age = 0.46(0.30–0.72) p = 0.001; model adjusted also for time breastfead and SEP did not converge.

For children of mothers with HIV infection, the PR of incomplete DTP vaccination would be expected to increase by a factor of, 2.03 (95%CI: 1.58–2.61) after adjustment for age and social class. Children of HIV-seropositive mothers were less likely to miss vaccination for MMR than those born to HIV negative mothers, with a PR of 0.46 (95%CI: 0.30–0.72).

Discussion

In our study population, 93% of children received the first dose of DTP-HB/Hib (DTP1) vaccine, while only 29% received the second dose (DTP2) and 30% the third dose (DTP3). By comparison, in other sub-Saharan countries like Zambia up to 79% of children received DTP3.¹² However, large variations have been observed, depending on the country and the vaccine considered; for example, an immunization coverage of 77.4% was reported in Kenya (all vaccines),¹³ while only 26.1% in rural Uganda (all vaccines),¹⁴ and of 41% in Nigeria (OPV).¹⁵

Actually, DTP3 coverage is a good indicator of the strength of routine immunization services.¹⁶ The differences observed across the studies may be explained by differences in socioeconomic environments (distance of health center from villages, quality of transportation and road condition), lifestyles, and the characteristics of the mothers (i.e., household wealth, marital status, age).¹⁷ For example, mothers living in informal urban settlements may attend the center to give birth but then go back to neighboring villages distant hours walking, and their children may not attend follow-up visits and subsequent vaccinations, especially if very poor. This results in a good coverage for BCG-OPV1 and DTP1 vaccine but then in a low coverage for DTP2, DTP3, and measles immunization, with the final outcome of an incomplete and inefficacious vaccination coverage for Diphtheria, Pertussis, Tetanus, and Polio. In addition, this population has little recognition from the government and is marginalized with regards to the provision of basic services, such as vaccination services, which may explain the low vaccination coverage.

In our study, there was no difference between children born to HIV-positive and HIV-negative mothers with regard to DTP1, while children born to HIV-positive mothers were twice more likely to be incompletely vaccinated than those born to HIV-negative mothers. Other studies carried out in Africa found that children born to HIV-infected mothers had lower immunization coverage than those born to HIV-negative mothers,^14,18 and even that HIV seropositive children were more likely to be incompletely vaccinated than their seronegative pairs.^12,19 To this regard, HIV seropositive children may be more likely to be hospitalized than other children and miss appointments at times when their immune system is suppressed. It is also possible that doctors and parents may tend not to immunize HIV positive children to avoid complications from vaccination.²⁰ However complications are limited to replicating live attenuated vaccines and are quite rare.^21-23 Nevertheless, misconceptions about immunization of HIV-infected children among parents may hinder vaccination of HIV seropositive children. For example, in a study carried out in Uganda, it was found that children of mothers who were HIV-infected and knew about their serostatus had a lower probability of being immunized compared to peers.¹⁴

Vaccination coverage for measles appears to remain low (vaccination was received by 45% of the children), despite the recent measles epidemics in Niamey, which occurred between 1999 and 2003 and involved more than 10,000 children below 5 y of age,²⁴ and a number of vaccination campaigns promoted by the Government, WHO, and other international organizations. Measles control may be more challenging in regions with a high prevalence of HIV infection because placental transfer of maternal antibodies is impaired in HIV infected women.²³ For this reason, the WHO Global Advisory Committee on Vaccine Safety (GACVS) subgroup on immune deficiencies, advice that children of HIV-infected women, should be vaccinated, regardless of their own HIV infection status, in areas where the burden of measles is high.²³ Remarkably, we observed that children born to HIV infected mothers were more likely to receive MMR vaccination than those born to the HIV seronegative. However, given the low coverage for measles on the all, this may indicate that MMR vaccines were not regularly available in the community apart from those provided to children born to HIV positive mothers.

BCG-OPV vaccination coverage did not vary by HIV status. Similar results were obtained in other African studies.¹⁸ Almost all the children included in our study received BCG-OPV vaccination within the first week after birth in keeping with the WHO recommendations, which, in order to keep vaccine coverage high, advice to administer the first dose of hepatitis B, BCG, and OPV vaccines at birth in high risk countries.^25,26 As confirmed also by our study, many developing countries have endorsed this recommendation in their vaccination schedules.^25-29

We did not find a positive relationship between maternal education and vaccination status. However, studies carried out in African countries found that maternal education is associated with health care knowledge, increased compliance to prevention and infants' vaccination uptake.^5,30-34 In addition, maternal education is related to household wealth and this affects food security and differentials in health. How inequalities affects health is well documented in African countries and elsewhere.^35,36 Such inequalities persist within the family structure, where children of older women are more privileged than younger ones and perhaps more likely to receive vaccination.^37,38

Our study has some possible limitations. First, a large part of vaccination data was based on maternal recall. This could bias RR of vaccination adherence away from the null hypothesis if HIV seropositive mothers were less likely to recall vaccination than their seronegative counterparts. Second, some HIV-positive children would have died in the first few months of life. This could potentially bias RR toward the null reducing the apparent effect of HIV serostatus on vaccination adherence. To reduce the effects of possible biases, analyses for DTP2 and DTP3 were restricted to relevant age-groups (i.e., children >3 months for DTP2, children >6 months for DTP3). Third, mothers of children less than 36 months old attending the health center of the Magama Foundation (Non-Governmental Organization: NGO) were recruited using convenience sampling. It is possible that very poor people were less likely to participate in the study; nevertheless, our results suggest little evidence of an association between maternal education and vaccination status. Unfortunately, we did not have information about other socio-economic variables such as household wealth. However people attending the Magama Foundation health center were altogether very poor, with small variations in their socioeconomic position. Fourth, since the study was not community-based, a recruitment bias determining an overestimation of coverage rates was likely to occur. Fifth, child HIV status was used as a proxy for mother’s HIV status; thus the women status was only indirectly deduced. This can be a source of bias for the study, as HIV positive mothers can give birth to HIV negative children if efficiently treated with antiviral drugs. However, this bias is unlikely to occur, since women living in this area had limited access to prenatal care and to antiretroviral therapy.

In conclusion, our results indicate that vaccine coverage among children born to HIV infected mothers was rather low; thus, it is important to favor access to vaccination programs in this population group. For this population, vaccination is of major importance because these children are at higher risk of developing infectious diseases. Benefits of vaccination out-weight potential adverse effects among HIV seropositive children.²¹ This information should be made available to both parents and clinicians in order to increase vaccination coverage in this highly vulnerable population group.

Methods

The Magama Foundation (Non-Governmental Organization: NGO) offers free services to orphans and other children born to disadvantaged and/or HIV positive women in the commune I, Koira Tégui, which is one of the 3 municipalities of the Urban Community of Niamey with a population of about 300,000 inhabitants (compared with 1,033,295 of all the city).¹¹

A convenience sample of mothers of children less than 36 months old, attending the health center of the Magama Foundation (Non-Governmental Organization: NGO), was recruited between January and March 2010. Overall, 502 mothers were enrolled in the study, the women were interviewed by a doctor, in the examination room, to obtain family’s socio-demographic information, knowledge of vaccination schedules and vaccine-preventable diseases, history of vaccinations received by their child, and breastfeeding. Information on the child HIV serostatus was also obtained. The mothers were assumed to be infected if the child was HIV-seropositive, independently of the child’s age; if a seronegative child was older than one year and had not repeated the test, the mother was assumed to be HIV-negative.

Mothers were required to give informed consent to the interview, in accordance with the ethical rules established by the local Ministry of Health, which authorized the study. Unvaccinated and partially vaccinated children were referred to vaccination centers to complete their schedule. The vaccination schedule included Bacille Calmette Guerin (BCG), oral polio (OPV) and diphtheria, tetanus and pertussis (DTP), first dose, at birth, and at 6, 10, and 14 weeks, hepatitis B (HB), haemophilus influenzae type B (Hib), measles and yellow fever at 9 months of age.

Data were checked for outliers, duplicate records, and distribution of the variables. Age, computed by date of examination minus date of birth, was analyzed as a categorical (0-5; 6-23; 24-36 months) variable. We examined the association between vaccination adherence (unvaccinated was the reference category) and mother’s HIV serostatus (exposure) using a log binomial regression. PRs and 95% confidence intervals (CIs) for vaccination adherence were computed.

We investigated for the presence of a clinically meaningful relationship between the potential confounders and the exposure and between the potential confounders and the outcome, compared stratum-specific estimates one another and with the crude estimate to identify effect modifiers and assessed the magnitude confounding by comparing the adjusted and crude estimates and their confidence intervals.

The magnitude of potential confounding factors was estimated by fitting a model with and without the variable of interest and by comparing the adjusted and crude estimates. Records with missing values for a variable were excluded for each analysis involving that variable.

To calculate vaccine coverage, the analysis was restricted to children >3 months for DTP2, to those >6 months for DTP3, and to >9 months for MMR (Measles, Mumps, Rubella). All children entered the analysis for BCG. Statistical analysis was carried out in STATA 13 software (StataCorp).

Disclosure of Potential Conflicts of Interest

All of the authors fulfill the authorship criteria and none of the authors have a financial relationship with any commercial entity that could have an interest in the subject of this manuscript.

Acknowledgments

We thank the Magama Foundation in Niamey, particularly the first Lady Hadjia Larba Tandja Founding President and CISP (The International Committee for the Development of Peoples) for supporting this work. We wish to thank Luca Avellis for his contribution to the editing of the manuscript.