http://www.diva-portal.org
This is the published version of a paper published in AIDS Care.
Citation for the original published paper (version of record):
Abraha, A., Myléus, A., Byass, P., Kahsay, A., Kinsman, J. (2019)
The effects of maternal and child HIV infection on health equity in Tigray Region, Ethiopia, and the implications for the health system: a case-control study
AIDS Care, 31(10): 1271-1281
https://doi.org/10.1080/09540121.2019.1601670
Access to the published version may require subscription. N.B. When citing this work, cite the original published paper.
Permanent link to this version:
Full Terms & Conditions of access and use can be found at
https://www.tandfonline.com/action/journalInformation?journalCode=caic20
AIDS Care
Psychological and Socio-medical Aspects of AIDS/HIV
ISSN: 0954-0121 (Print) 1360-0451 (Online) Journal homepage: https://www.tandfonline.com/loi/caic20
The effects of maternal and child HIV infection on
health equity in Tigray Region, Ethiopia, and the
implications for the health system: a case–control
study
Atakelti Abraha, Anna Myléus, Peter Byass, Asmelash Kahsay & John
Kinsman
To cite this article: Atakelti Abraha, Anna Myléus, Peter Byass, Asmelash Kahsay & John Kinsman (2019) The effects of maternal and child HIV infection on health equity in Tigray Region, Ethiopia, and the implications for the health system: a case–control study, AIDS Care, 31:10, 1271-1281, DOI: 10.1080/09540121.2019.1601670
To link to this article: https://doi.org/10.1080/09540121.2019.1601670
© 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group
Published online: 08 Apr 2019.
Submit your article to this journal
Article views: 855
View related articles
The e
ffects of maternal and child HIV infection on health equity in Tigray Region,
Ethiopia, and the implications for the health system: a case
–control study
Atakelti Abraha a,b, Anna Myléusc, Peter Byass c,d,e, Asmelash Kahsayfand John Kinsman c,g
a
Tigray Health Bureau, Tigray, Ethiopia;bEthiopian Health Insurance Agency, Addis Ababa, Ethiopia;cDepartment of Epidemiology and Global Health, Umeå University, Umeå, Sweden;dInstitute of Applied Health Sciences, School of Medicine and Dentistry, University of Aberdeen, Aberdeen, UK;eMRC/Wits Rural Public Health and Health Transitions Research Unit, School of Public Health, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa;fMicronutrient initiative, Tigray, Ethiopia;gDepartment of Public Health Sciences, Global Health (IHCAR), Karolinska Institutet, Stockholm, Sweden
ABSTRACT
Services that aim to prevent mother-to-child HIV transmission (PMTCT) can simultaneously reduce the overall impact of HIV infection in a population while also improving maternal and child health outcomes. By taking a health equity perspective, this retrospective case control study aimed to compare the health status of under-5 children born to HIV-positive and HIV-negative mothers in Tigray Region, Ethiopia. Two hundred and thirteen positive women (cases), and 214 HIV-negative women (controls) participated through interviews regarding their oldest children. Of the children born to HIV-positive mothers, 24% had not been tested, and 17% of those who had been tested were HIV-positive themselves. Only 29% of the HIV-positive children were linked to an ART programme. Unexpectedly, exposed HIV-negative children had fewer reports of perceived poor health as compared to unexposed children. Over 90% of all the children, regardless of maternal HIV status, were breastfed and up-to-date with the recommended immunizations. The high rate of HIV infection among the babies of HIV-positive women along with their low rates of antiretroviral treatment raises serious concerns about the quality of outreach to pregnant women in Tigray Region, and of the follow-up for children who have been exposed to HIV via their mothers.
ARTICLE HISTORY
Received 11 April 2018 Accepted 21 March 2019
KEYWORDS
HIV; under-5 mortality; under-5 morbidity; PMTCT; health equity; Ethiopia
Introduction
A range of factors influences children’s health, not least of which is their parents’ own health status (CSDH,
2008). Maternal HIV-positive status is a particularly significant driver of child health inequities for both biological and social reasons. Biologically, children born to HIV-positive mothers have a 15% to 45% risk of acquiring HIV in the absence of treatment (WHO,2018), and this can expose the child to numer-ous adverse health outcomes, including premature mortality (WHO, 2010). Socially, children born to HIV-positive mothers face a higher risk of death, as well as poorer access to education and health services, due to the death of one or both parents (Guo, Li, & Sherr, 2012), or inadequate nutrition (Mkwanazi, Rochat, & Bland, 2015).
Since an HIV diagnosis during pregnancy should lead to a woman being put on treatment, PMTCT pro-grammes improve child health both biologically – through reducing mother-to-child transmission of HIV
to below 5%– and socially, through improving maternal health. In Ethiopia, the prevention of mother-to-child transmission (PMTCT) programme was initiated in 2001. Current PMTCT guidelines (Ethiopian Federal Ministry of Health,2014) follow the WHO recommen-dation (World Health Organization,2010), whereby all pregnant and breastfeeding women receive antiretroviral therapy (ART) immediately after diagnosis, irrespective of the clinical stage of disease or CD4 count. This facili-tates both a reduction in HIV-related morbidity and mortality for the woman herself, and also a reduction in the risk of her passing HIV to her baby. All infants who are born to infected mothers (i.e., HIV-exposed infants) receive antiretroviral (ARV) prophy-laxis, which includes Nevirapine once daily for six weeks, after which they are tested– at six weeks of age or at the earliest opportunity thereafter– using polymer-ase chain reaction (PCR). Infants with a positive virolo-gical test result start ART immediately, following which they have a monthly follow up for thefirst six months of
© 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/ 4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.
CONTACT John Kinsman john.kinsman@umu.se Department of Epidemiology and Global Health, Umeå University, SE-901 87 Umeå AIDS CARE
2019, VOL. 31, NO. 10, 1271–1281
life, and then every three months. A confirmatory HIV test is administered at 18 months.
In 2005, there were nine PMTCT and four compre-hensive ART-providing health facilities in Tigray Region in northern Ethiopia, and this had expanded to 142 PMTCT and 77 ART service-providing health facilities by 2016. This represents a coverage rate of 67% and 34% respectively in the Region. In 2009 Tigray Regional Laboratory started to provide Early Infant Diagnosis through polymerase chain reaction (PCR) HIV testing service for the region (Ethiopia Public Health Institute,
2017).
Substantial reductions in HIV prevalence in adult and pregnant women have been achieved since the peak in 2001. The current adult HIV prevalence in Ethiopia is considered low, 1.5% at national level, but there are also substantial variations in the rates of mother-to-child HIV transmission in different parts of Ethiopia, ranging from 15% in Dire-Dawa (Wudineh & Damtew,
2016) to 8.2% in Addis Ababa (Mirkuzie, Sisay, Hinder-aker, Moland, & Mørkve,2012; Negash & Ehlers,2016). In Tigray Region, the HIV prevalence rate is 1.8%, though with wide differences by residence (4.2% in urban to 0.6% in rural) and sex (1.9% in women and 1% in men) (EDHS, 2016). These are caused by, among other issues, differential access to health care, and low ante-natal care (ANC) and skilled delivery cov-erage (Barnabas, Pegurri, Selassie, Naamara, & Zemar-iam,2014; United Nations,2015).
In spite of these low overall rates, however, there were still an estimated 33,200 pregnant women and more than 200,000 children under the age of 15 living with HIV in Ethiopia in 2013 (Federal Ministry of Health Ethiopia,
2014). These figures reflect the situation in a number of other African countries (Landes et al.,2012; Ndirangu, Newell, Tanser, Herbst, & Bland,2010), where mother-to-child transmission of HIV continues to take place in spite of the availability of PMTCT services.
The post-2015 Sustainable Development Goals (SDG) agenda emphasizes equity as a cross-cutting theme for health and other development-related spheres. Child health is specifically identified in SDG 3, with targets on neonatal and under-5 mortality that, if achieved, would bring about equitably low rates of mortality among children globally (UN DSD,2017). Ethiopia has identified child health inequity as an issue of concern, and has put in place strategies to address the problem in its current 2015–2020 health sector transformation plan (Mullan,2016).
In order to understand the effect of policies to reduce child mortality, evaluations of services are needed in order to facilitate an informed decision-making process for health service provision based on local conditions.
The aim of this paper, therefore, is to assess the health outcomes of children born to mothers (both HIV-posi-tive and HIV-negaHIV-posi-tive) enrolled in the PMTCT service in Tigray Region, Ethiopia, as a means of providing evi-dence for improving child health services and thereby promoting child health equity within the context of the Sustainable Development Goals.
Methods
Study design and setting
This retrospective case–control study was performed from July-August 2014 in the South-Eastern Zone of Tigray Region, North Ethiopia. The Zone comprises four admin-istrative woredas (Districts) surrounding Mekelle, the capital of Tigray Region (Figure 1), where an estimated 600,000 people live (Figure 1). The people of the Zone live under broadly similar socio-economic and cultural conditions. More than 80% of the population are farmers with the remainder living in semi-urban small towns.
No woreda-specific HIV prevalence data exists in Tigray Region. However, it is known that more than half of the HIV-positive pregnant women in the Region do not receive PMTCT or enrol in ART due to low ANC and skilled delivery coverage, and also to poor linkages and adherence to ART.
There are 32 health centres, 4 primary hospitals and 72 health posts (the lowest level of health facility in the Ethiopian health system) within the South-Eastern Zone of Tigray. At health posts, preventive maternal and child services are provided, including treatment for selected diseases and HIV testing and counselling. Health centres and hospitals provide skilled delivery and PMTCT services integrated within antenatal care (ANC). In the health centres, all women are offered free HIV testing and counselling during ANC and deliv-ery, and referral to the nearest hospitals for initiation of ART services if the infection is confirmed. Health centres provide ARV prophylaxis during ANC and delivery, as well as follow-up for mothers and exposed infants, including through the collecting and transporting of dried blood samples from HIV-exposed infants for test-ing at the Regional laboratory up until the age of 18 months.
Sampling methods
The South-Eastern Zone was randomly selected from among the seven Zones in Tigray Region, and all HIV-positive women who received PMTCT and enrolled in ART care in the pastfive years in the four woredas in the Zone were included in the study.
We used the ART registry in the four primary hospitals to identify HIV-positive women, the year of pregnancy, and details of their residence at kebele or village level. Sim-ultaneously, we used the follow-up register for pregnant women at the health posts to identify HIV-negative from the same kebele and the same year of pregnancy. By combining these two datasets, it was possible to ident-ify under-5 year children born to HIV-positive women– who would be taken as the cases– and under-5 year chil-dren born to women who had not been diagnosed with HIV, who would be taken as the control group (Figure 2). Data collectors contacted each of the HIV-positive mothers in order to identify all the children who had been born during the five years prior to the study (whether alive or dead at the time of interview). For the control group, households were randomly selected from the list of mothers whose most recent HIV test had been negative, ensuring a proportion of 1:1 for cases and controls. Under-5-year-old children of these mothers who had been born during thefive years prior to the study (whether alive or dead) were then identified. In cases where more than one under-5 child had been born during that period, only the oldest identified child was included in the analysis.
A structured questionnaire was prepared by thefirst author (AA) that included items on maternal health,
socio-demographic status, economic and reproductive history, child mortality and morbidity, and utilization of child health services. The questionnaire was prepared in English, translated to the local language, Tigrinya, pre-tested in a non-study area, and revised accordingly.
In each woreda,five contracted employees of the ART sites– “HIV case managers”, who are trained to ensure ART adherence and who have the contact addresses of patients for follow-up – collected the data under the supervision of an ART nurse. Data collectors and super-visors received three-day training on data collection, confidentiality, ethics, and supervision skills. Data collec-tors used the information collected from the ART regis-try to approach women at their home, and to trace the addresses of women who had changed their place of resi-dence. In the event that the mother was deceased, the child’s caregiver was interviewed.
Data were submitted daily to supervisors and checked for completeness and quality using a checklist. Addition-ally, the first author and one skilled coordinator re-checked a randomly selected 10% sample of the dataset that had been approved by the supervisors on a weekly basis. Incomplete, unreliable or inappropriate data ident-ified during checking, rechecking and during data entry were returned for clarification and/or additional infor-mation as required.
Figure 1.Map of Tigray Region, Ethiopia, study areas highlighted in light blue.
Data analysis
Data were summarized and analysed using PASW Stat-istics version 21.0 (SPSS Inc., Chicago, IL). Chi-square tests and Fishers exact test were used to compare the health status and other relevant variables of under-5 chil-dren born to HIV-positive and HIV-negative mothers. Bivariate and multivariate logistic regressions analyses were performed for variables with statistically significant association (p-value < .05).
Ethical considerations
The study received ethical approval from Mekelle Univer-sity College of Medical Sciences and the Regional Research Review Committee of Tigray Regional Health Bureau. To protect the confidentiality of participants, data collectors were specifically selected as health pro-fessionals who are already aware of the HIV status of the study subjects, and who had already been trained to keep all such information confidential. The data collection process used verbal informed consent and respected the right of the study subjects to decline from participating.
Results
Characteristics of respondents and children
A total of 247 HIV-positive women (cases) who received PMTCT and who were currently enrolled in ART care were identified from the register. During the actual data
collection, 19 (7.7%) women were not found and 9 (3.9%) declined to participate; the remainder (213/247) participated to give an overall response rate of 86.2%. Among the selected 247 HIV-negative women (controls), 12 (4.9%) declined to participate and 7 (2.8%) had, since their initial HIV-negative test, been diagnosed with HIV. These were substituted with the next, randomly assigned woman on the list. The remaining (228/247) were willing to participate, giving an overall response rate of 93%.
A total of 213 HIV-positive and 214 HIV-negative mothers participated in the study (Table1), through whom we received details of the health outcomes of 427 children (213 born to HIV-positive mothers, defined below as “exposed”; and 214 born to women without an HIV diagnosis, defined below as “unex-posed”). Twenty-five mothers had more than one surviv-ing under-5-year-old child, but only the eldest child in these cases was included in the study.
Most of the socio-economic and reproductive charac-teristics of cases and controls and their children were comparable, but significant differences (P < .05) were found in respondents’ age, marital status, occupation, and the number of pregnancies. HIV-positive women tended to be older, more likely to be divorced or self-employed, and have higher parity (Table 1).
Child HIV status
A total of 162 (76%) out of the 213 exposed children had themselves been tested for HIV, while the remaining 51
(24%) children, of whom 46 (90.2%) were older than four weeks (and therefore eligible for HIV testing) had unknown HIV status – this was either because they had not been tested (for any of a variety of reasons), or because the mothers or caregivers did not remember if they had been tested (Table 2). Of those who had been tested, 134 (83%) were found to be HIV-negative, and 28 (17%) were positive. Only 8 (29%) of the HIV-positive children were linked to an ART programme. Delivery at home or at a health post attended by unskilled or traditional attendants, as opposed to deliv-ery at health centre and Hospital by skilled health workers, was a significant risk factor for increased risk of HIV infection of the new-born [adj OR 3.9 (95% CI 1.7–9.1, p-.002)].
Mortality
A total of 32 (7.5%) of the 427 babies born were reported to have died, 24 of whom had been exposed to HIV, and 8 of whom had been unexposed (Table 2). There was no significant difference in sex and age at death; however, more than 93% of the mortality occurred before 2 years of age, and 78% before thefirst birthday. On univariate analysis, maternal HIV-positive status, not receiving uptake of antenatal care during pregnancy, delivery at home or at health post, low maternal income status, and child’s HIV-positive status were all found to be sig-nificant risk factors for mortality (p < .01) (Table 3).
However, when adjusted for maternal age, marital sta-tus, occupation, number of pregnancy, child HIV status and variables that were significant at the <.05 level in the univariate analysis, and when exposed children with unknown HIV status are removed, home or health post-delivery and HIV infection remained as significant predictors of child mortality. These contributed to six fold [adj OR 6.2 (95% CI 2.2–17.3, <.001)] and fivefold [adj OR 5.2 (95% CI 1.5–18.0, p-.009)] increases respect-ively (Table 4).
Morbidity
On univariate analysis, occupation, antenatal care, place of birth and child HIV were significant risk factors (p < .03) for perceived child morbidity. When adjusted for maternal characteristics that showed asignificant differ-ence (as inTable 4), the following remained as significant
factors for perceived poor health: HIV infection [adj OR 3.3 (95% CI 1.1–10.0, p = .03)], and delivery attended by unskilled attendants at home or at a health post [adj OR 2.9 (95% CI 1.4–6.0, p = .005).
Exposed but uninfected children are perceived to have better health status than unexposed children [adj OR 0.4 (95% CI 0.1–0.9, p = .04)]. Despite this, there was no sig-nificant difference between exposed and unexposed chil-dren with regard to those who experienced at least one episode of diarrhoea, fever or cough with fast breathing during the past two months (Table 5).
Table 1.Socio-demographic, economic and reproductive characteristics of respondents by HIV status.
Indicator Response N (%) HIV-positiven (%) HIV- negativen (%) P-value Maternal survival Surviving 422(98.8) 211(99.0) 211(98.6) .5
Dead 5(1.2) 2(1.0) 3(1.4)
Age 15–24 years 115(26.9) 34(15.9) 81(37.8) <.001* 25–34 Years 245(57.4) 142(66.7) 103(48.1)
> 34 years 67(15.7) 37(17.4) 30(14.1)
Marital status Married 312(73.1) 136(63.8) 176(82.2) <.001*
Single 28(6.6) 19(8.9) 9(4.2)
Divorced 63(14.8) 43(20.1) 20(9.4)
Widowed 24(5.6) 15(7.0) 9(4.2)
Educational status Illiterate 284(66.5) 147(69.0) 137(64.0) .2 Elementary 100(23.4) 50 (23.5) 50(23.4)
High school plus 43(10.1) 16(7.5) 27(12.6)
Occupation Housewife 162(37.9) 71(33.3) 91(42.5) .001* Farmer 170(39.8) 91(42.7) 79(36.9)
Employed 27(6.3) 7(3.3) 20(9.3)
Self Employed 68(15.9) 44(20.7) 24(11.2)
Religion Orthodox Christian 412(96.5) 207(97.2) 205(95.8) .4
Muslim 15(3.5) 6(2.8) 9(4.2)
Income status Lower 114(26.7) 64(29.9) 50(23.3) .1
Fair/Good 313(73.3) 149(70.1) 164(76.7)
Number of pregnancies One 340(82.5) 164(77.7) 176(87.6) .03*
Two 65(15.8) 42(19.9) 23(11.4)
Three 7(1.7) 5(2.4) 2(1.0)
Total children Less than 4 326(72.1) 152(48.6) 161(51.4) .4 4 and above 126(27.9) 61(53.5) 53(46.5)
Household size Less than 5 338(74.8) 157(48.5) 167(51.5) .3 5 and above 114(25.2) 56(54.4) 47(45.6)
Table 2.Characteristics under-5-year-old children by child indicators. Indicator Response N (%) Exposed (N = 213) n (%) Unexposed (n (%)N = 214) P-value Survival Surviving 395(92.5) 189(88.7) 206(96.3) <.001* Dead 32(7.5) 24(11.3) 8(3.7)
Age Less than 1 month 13(3.0) 10(4.7) 3(1.4) .1
1–12 month 137(32.1) 71(33.3) 66(30.8) Above 12 months 277(64.9) 132(62.0) 145(67.8)
Mean age (±SD) 23.2(±17.7) 21.1(±13.6) .2
Sex Male 226(52.9) 118(55.4) 108(50.5) .4
Female 201(47.1) 95(44.6) 106(49.5)
Breast Feeding Breast fed 420(98.4) 209(98.1) 213(99.5) .3 Not breast fed 7(1.6) 4(1.9) 1(0.5)
Immunization to their agea Completed 359(90.9) 174(92.1) 185(89.8) .4
No/not adequate 36 (9.1) 15(7.9) 21(10.2)
Antenatal care visits None 53(12.4) 30(14.1) 23(10.7) .4 At least once 359(84.1) 181(85.0) 178(83.2)
Not known 15(3.5) 2(0.9) 13(6.1)
Place of birth Home/health post 163(38.2) 60(28.2) 103(48.1) <.001* Hospital/Health centre 264(61.8) 153(71.8) 111(51.9)
HIV status HIV infected 28(13.2) 28(13.2) NA <.001* HIV status unknown 51(23.9) 51(23.9) NA
HIV uninfected 134(62.9) 134(62.9) NA
Unexposed 214(100) NA 214(100)
Abbreviations: SD = standard deviation, NA = not applicable.
a
Deceased children excluded.
Table 3.Comparison of 24 exposed and 8 un-exposed deceased under-5-year-old children by maternal and child indicators.
Indicators Response N (%)
Exposed
n (%) Unexposedn (%) P-value Age of respondent 15–24 years 115(26.9) 4(16.7) 1(12.5) .16
25–34 years 245(57.4) 14(58.3) 5(62.5) 35–49 years 67(15.7) 6(25.0) 2(25.0)
Marital status Married 312(73.1) 13(54.2) 6(75.0) .09
Single 28(6.6) 1(4.2) 0(0.0)
Divorced 63(14.8) 8(33.3) 1(12.5)
Widowed 24(5.6) 2(8.3) 1(12.5)
Religion Orthodox Christian 412(96.5) 22(91.7) 8(100.0) .38
Muslim 15(3.5) 2(8.3) 0(0.0)
Educational status Illiterate 284(66.5) 18(75.0) 8(100.0) .16 Elementary 100(23.4) 6(25.0) 0(0.0)
High school plus 43(10.1) 0(0.0%) 0(0.0)
Occupation House wife 162(37.9) 7(29.2) 2(25.0) .19
Farmer 170(39.8) 10(41.7) 6(75.0)
Employed 27(6.3) 0(0.0%) 0(0.0)
Self employed 68(15.9) 7(29.2) 0(0.0)
Number of pregnancies One 340(82.5) 15(62.5) 4(50.0) <.001
Two 65(15.8) 6(25.0) 4(50.0)
Three 7(1.7) 3(12.5) 0 (0.0)
Total children Less than 4 313(73.3) 19(79.2) 4(50.0) .2 4 and above 114(26.7) 5(20.8) 4(50.0)
Household size Less than 5 324(75.9) 19(79.2) 4(50.0) .6 5 and above 103(24.1) 5(20.8) 4(50.0)
Antenatal care visits None 53(12.4) 9(37.5) 1(12.5) .004* At least once 359(84.1) 15(62.5) 7(87.5)
Income status Lower 114(26.7) 13(54.2) 1(12.5) .04*
Fair/Good 313(73.3) 11(45.8) 7(87.5)
Place of birth Hospital/Health centre 264(61.8) 6(25.0) 1(12.5) <.001* Home/Health Post 163(38.2) 18(75.0) 7(87.5)
Child HIV status Infected 28(13.2) 8(25.0) NA <.001*
Uninfected 51(23.9) 12(37.5) NA
Unknown status 134(62.9) 4(12.5) NA
Unexposed 214(100) NA 8 (25.0)
Abbreviation: NA = not applicable. *Significant association.
Utilization of child health services
Utilization of child health services was comparable in both exposed and unexposed children. Over 92% of all HIV-exposed children and 90% of unexposed children were up-to-date with the recommended immunizations; more than 98% in both groups had been breastfed at least for some time (Table 2); and more than 60% of children in both groups (61.8% exposed and 61.2% unexposed) visited a health facility for treatment as necessary. No significant difference was found in the proportions of exposed and unexposed children making at least one visit to a health facility after adjusting for maternal variables (Table 5).
Discussion
Our study found that in spite of the well-established PMTCT programme that has been running in Tigray Region since 2001, 24% of exposed infants had unknown HIV status, which is broadly line with previous studies that have reported poor access to HIV testing and care for children in Ethiopia (Kebede, Gebeyehu, Jain, Sun, & Haubrich, 2014). Among those tested for HIV, 28 (17%) of the babies born to HIV-positive mothers– 11 (39.3%) of whose deliveries took place a health facility – were themselves HIV-infected. The rate of HIV in chil-dren is substantially higher than both the 5% rate
achieved in South Africa (Goga et al.,2015Grimwood, Fatti, Mothibi, Eley, & Jackson,2012) and in other recent studies conducted in Ethiopia, where infection rates of 10% (Kassa,2018) and 6% were found in Addis Ababa (Negash & Ehlers,2016). Further, of these 28 children, only 8 (29%) had been linked to an ART programme. This means that more than 70% of the HIV-positive under-5-year-old children in our sample were at serious risk of disease and early death. This highlights the need for significantly improved awareness and integration of PMTCT within other home-based services.
Thefindings on mortality were broadly in line with expectations. Overall under-5 year child mortality in our study was consistent with the recent Ethiopian Demographic and Health Survey (DHS) (CSA, 2016), and mortality among children with HIV was much higher than it was among those who were not infected. Unlike many studies from the early days of national PMTCT programmes in Africa (Kuhn et al., 2005; Nakiyingi et al., 2003; Newell et al., 2004; Zaba et al.,
2005) as well as from some more recentfindings (Kur-ewa et al.,2010; Naniche et al.,2009), ourfindings indi-cate that exposure to maternal HIV alone is not a risk factor for under-5 year child mortality. However, deliv-ery attended by an unskilled person at home or at a health post, and child HIV infection, are both significant risk factors. This is all in line with previous studies that have pointed to a higher risk of mortality among HIV-infected children (Violari et al.,2008), as well as research indicating that delivery in a well-equipped health insti-tution is a predictor of improved maternal and child out-comes, regardless of maternal HIV status (Chinkhumba, De Allegri, Muula, & Robberstad,2014; Moyer, Dako-Gyeke, & Adanu,2013).
In spite of the high mortality rate among HIV-exposed children, it is important to note that many chil-dren, both HIV-infected and not, do survive; but in all cases, the health system needs to be responsive to the particular health and psychosocial needs of children raised in families affected by HIV. Good outcomes can be attained through provision of PMTCT services, sup-porting long term ART treatment for the mother, and counselling about child feeding (Lerebo, Callens, Jack-son, Zarowsky, & Temmerman,2014; Tura, Fantahun, & Worku,2013; Wudineh & Damtew,2016).
Elements of thefindings relating to morbidity were also in line with expectations, with episodes of diarrhoea, fever and cough with fast breathing in our study being consistent with the latest Ethiopian DHS report (CSA,2016). Further, HIV-infected children exhibited much higher levels of morbidity than the HIV-uninfected children, as expected. Viewing this through an equity lens raises questions about how the HIV-positive children could be better served
Table 4.Bivariate and multivariate analyses of risk factors for under-5-year-old child mortality.
Indicator n (%) Unadjusted OR (95% CI) Adjusted OR (95% CI) P-value Maternal HIV statusa Positive 24(75.0) 3.8(1.4–7.5) 2.6(0.8–7.7) .1 Negative 8(25.0) 1 1 Antenatal care visit None 10(31.3) 3.6(1.6–8.0) 1.5(0.6–3.7) .4 At least once 22(68.8) 1 1 Place of delivery Home/ Health Post 25(78.1) 6.7(2.8–15.8) 6.2(2.2–17.3) <.001* Hospital/Health centre 7(21.9) 1 1 Income status Lower 14(43.8) 2.6(1.2–5.4) 1.8(0.8–4.0) .2 Fair/Good 18(56.3) 1 1
Child HIV statusb,c
Infected 8(25.0) 10.3 (3.5–30.4) 5.2(1.5–18.0) .009* Uninfected 12(37.5) 2.5(1.0–6.4) 2.6(0.9–7.2) .07 Unexposed 8(25.0) 1 1
Abbreviations: OR = odds ratio, CI = confidence interval. *Significant difference.
a
Adjusted for all variables in the table except for child HIV status including maternal age, mariatal statu, number of pregnancy in thefive years prior to study and occupation.
bAdjusted for all variables in the table except for maternal HIV status,
includ-ing maternal age, mariatal status, number of pregnancy in thefive years prior to study and occupation.
c
Exposed children with unknown HIV status removed.
by the health system, including, perhaps, through the pro-vision of nutritional supplementation.
While previous reports indicate exposure to maternal HIV alone as a risk factor for childhood mor-bidity (Koyanagi et al.,2011; Marquez et al.,2014), our results showed that morbidity was significantly lower in exposed but uninfected children. This encouraging finding may be explained by the counselling that HIV-positive mothers receive during treatment fol-low-up and antenatal care, but it may also be a product of the co-trimoxazole prophylaxis that is provided for
exposed children (Homsy et al., 2014; Kourtis et al.,
2013).
The uptake of immunization services alongside good rates of breastfeeding were consistent with thefindings of the Ethiopian DHS (CSA, 2016). Unlike one study from South Africa (Ndirangu, Bärnighausen, Tanser, Tint, & Newell,2009), our study found no difference in
access to child health care and services, breastfeeding, and uptake of immunization between exposed and unex-posed children. Thesefindings were to be expected given the free access to health care to all children born to
HIV-Table 5.Health status, episodes of morbidity and health service utilization surviving under-5-year-old children two months prior to the study.
Indicators Yesn (%)
Unadjusted Adjusted
OR (CI 95%) P-value OR (CI 95%) P-value Reported poor health
Child HIV statusa,b
Infected 9(19.1) 4.6(1.8–12.0) .002 3.3(1.1–10.0) .03* Uninfected 7(14.9) 0.3 (0.1–0.8) .01 0.4(0.1–0.9) .04* Unexposed 31(66.0) 1 1 Occupation House wife 16(30.8) 2.8(0.6–12.8) .2 2.6(0.5–12.4) .2 Farmer 29(55.8) 5.1(1.2–22.8) .03 4.5(1.0–20.6) .05 Employee 4(7.7) 5.9(1.0–35.2) .05 6.1(1.0–38.2) .05 Self employed 3(5.8) 1 1 Antenatal care None 13(26.5) 2.3(1.0–5.3) .04 2.4(1.0–5.6) .05 At least once 36(73.5) 1 1 Place of birth Home/Health post 31(59.6) 2.2(1.1–4.4) .02 2.9(1.4–6.0) .005* Hospital/Health centre 21(40.4) 1 1 Episodes of Diarrhoea Maternal HIV statusa
Positive 32(16.9) 0.6(0.4–1.0) .04 0.6(0.4–1.2) .2
Negative 52 (25.2) 1 1
Child HIV statusa,b
Infected 6(30.0) 1.3(0.5–3.5) .6 1.3(0.5–3.7) .6
Uninfected 20(16.4) 0.6(0.3–1.0) .07 0.6(0.3–1.1) .1
Unexposed 52 (25.2) 1 1
Episode of Fever Child HIV statusa,b
Infected 7(35.0) 2.4(0.9–6.4) .08 2.0(0.7–5.8) .2
Uninfected 16(13.1) 0.7(0.4–1.3) .2 0.7(0.3–1.3) .3
Unexposed 38(18.4) 1 1
Cough with fast breath Child HIV statusa,b
Infected 2(10.0) 1.0(0.2–4.5) .9 1.3(0.3–6.9) .7 Uninfected 8(6.6) 0.7(0.3–1.5) .3 0.9(0.3–2.2) .8 Unexposed 20(9.7) 1 1 Income status Lower 14(40.0) 2.1(1.0–4.4) .04 2.2(1.0–5.0) .05 Fair/Good 21(60.0) 1 1
Visit to health facility Child HIV statusa,b
Infected 11(5.1) 0.7(0.3–1.9) .5 1.0(0.4–2.7) .9 Uninfected 78(35.9) 1.0(0.7–1.7) .7 1.1(0.7–1.9) .7 Unexposed 128(59.0) 1 1 Place of birth Home/Health post 77(30.6) 1.7(1.1–2.6) .02 0.6(0.4–1.0) .07 Hospital/Health centre 175(69.4) 1 1 Child age ≤ 1 year 96(38.1) 1.7(1.1–2.7) .02 0.6(0.4–1.0) .07 >1 year 156(61.9) 1 1
Abbreviations: OR = odds ratio, CI = confidence interval. *Significant difference.
aAdjusted for variables in each table and for maternal age, mariatal status, number of pregnancy in thefive years prior to study and occupation. b
positive women in the health system, the increasing acceptability of immunization, and the culture of breast feeding in Ethiopia, the latter of which is strongly sup-ported by the Ethiopian PMTCT strategy. It could also be a result of the ongoing good health and survival of HIV-positive women enrolled in ART programmes, as this can facilitate sustaining the household income.
Limitations of the study
We acknowledge that since the data was based on self-report, some biases could have been included, either through recall bias or a reluctance of the respondents to share sensitive personal information. However, this issue should have been limited by the fact that the data collectors were trained and experienced HIV case managers, who fully understood and practised the principle of confidentiality.
Conclusion
In spite of the well-established PMTCT programme that has been running in Tigray Region since 2001, 17% of the babies born to HIV-positive mothers were them-selves HIV-infected, and of these, only 29% were enrolled in an ART programme. These are poorer rates than expected, and they raise serious concerns about the quality of both outreach to pregnant women in Tigray Region, and of the follow-up of children who have been exposed to HIV via their mothers.
Viewing thesefindings through an equity lens provides the opportunity to ensure that the health system is more responsive to the needs of HIV-positive mothers and their children, whether infected themselves or not. Three broad areas of need have been identified: improvement in infant HIV testing; improvement in infant HIV treatment; and a reduction in infant HIV positivity rates. These issues can be addressed by enhancing the coverage of skilled delivery and PMTCT/ART services through decentralizing to health post level; integrating the follow-up of HIV-exposed children within community-level campaigns; and improving the capacity of health workers.
Acknowledgements
We thank the populations of the study woredas, the study
par-ticipants, and the woreda health offices for providing
per-mission, information and facilitation of the study. We also acknowledge the valuable input received from the reviewers.
Disclosure statement
At the time of this study, thefirst author (AA) was working as
Deputy Head of the Tigray Regional Health Bureau.
Funding
This work was primarily supported as part of the routine activities of the Tigray Regional Health Bureau. The authors thank the Swedish Research Council for Swedish Research Links collaboration grant C0615601 which facilitated external participation in this research.
Data availability
Since this study involves HIV-positive individuals, the data cannot be placed in the public domain because of the risk of identity disclosure.
ORCID
Atakelti Abraha http://orcid.org/0000-0002-8886-7199
Peter Byass http://orcid.org/0000-0001-5474-4361
John Kinsman http://orcid.org/0000-0003-1332-4138
References
Barnabas, G., Pegurri, E., Selassie, H. H., Naamara, W., &
Zemariam, S. (2014). The HIV epidemic and prevention
response in Tigrai, Ethiopia: A synthesis at sub-national
level. BMC Public Health.doi:10.1186/1471-2458-14-628
Central Statistical Agency [Ethiopia] and ICF International.
(2016). Demographic and health survey 2016 key indicators
report.
Chinkhumba, J., De Allegri, M., Muula, A. S., & Robberstad, B. (2014). Maternal and perinatal mortality by place of delivery in sub-Saharan Africa: A meta-analysis of population-based
cohort studies. BMC Public Health, 14(1), 1014. doi:10.
1186/1471-2458-14-1014
CSDH. (2008). Closing the gap in a generation. Health equity
through action on the social determinants of health. Final report of the Commission on Social Determinants of
Health, 246.doi:10.1080/17441692.2010.514617
EDHS. (2016). Ethiopia demographic and health survey 2016.
Addis Ababa: Central Statistical Agency (CSA) [Ethiopia] and ICF.
Ethiopia Public Health Institute. (2017). Ethiopia services
availability and readiness assessment report. Addis Ababa.
Federal Ministry of Health Ethiopia. (2014). Country progress
report on the HIV. Addis Ababa, Ethiopia.
Federal Ministry of Health Ethiopia. (2014). National
guide-lines for comprehensive HIV prevention, care and treatment. Addis Ababa.
Goga, A. E., Dinh, T.-H., Jackson, D. J., Lombard, C., Delaney, K. P., Puren, A.,… Pillay, Y. (2015). First population-level
effectiveness evaluation of a national programme to prevent
HIV transmission from mother to child, South Africa. Journal of Epidemiology and Community Health, 69(3),
240–248.doi:10.1136/jech-2014-204535
Grimwood, A., Fatti, G., Mothibi, E., Eley, B., & Jackson, D.
(2012). Progress of preventing mother-to-child
trans-mission of HIV at primary healthcare facilities and district hospitals in three South African provinces. South African
Medical Journal=Suid-Afrikaanse Tydskrif Vir
Geneeskunde, 102(2), 81–83.
Guo, Y., Li, X., & Sherr, L. (2012). The impact of HIV/AIDS on children’s educational outcome: A critical review of global
literature. AIDS Care – Psychological and Socio-Medical
Aspects of AIDS/HIV,doi:10.1080/09540121.2012.668170
Homsy, J., Dorsey, G., Arinaitwe, E., Wanzira, H., Kakuru, A.,
Bigira, V.,… Tappero, J. W. (2014). Protective efficacy of
prolonged co-trimoxazole prophylaxis in HIV-exposed chil-dren up to age 4 years for the prevention of malaria in Uganda: A randomised controlled open-label trial. The
Lancet Global Health, 2(12), e727–e736. doi:10.1016/
S2214-109X(14)70329-8
Kassa, G. M. (2018). Mother-to-child transmission of HIV
infection and its associated factors in Ethiopia: A systematic
review and meta-analysis. BMC Infectious Diseases,doi:10.
1186/s12879-018-3126-5
Kebede, B., Gebeyehu, A., Jain, S., Sun, S., & Haubrich, R. (2014). Delay in early infant diagnosis and high loss to fol-low-up among infant born to HIV-infected women in
Ethiopia. World Journal of AIDS, doi:10.4236/wja.2014.
44048
Kourtis, A. P., Wiener, J., Kayira, D., Chasela, C., Ellington, S.
R., Hyde, L.,… Jamieson, D. J. (2013). Health outcomes of
HIV-exposed uninfected African infants. AIDS (London,
England).doi:10.1097/QAD.0b013e32835ca29f
Koyanagi, A., Humphrey, J. H., Ntozini, R., Nathoo, K.,
Moulton, L. H., Iliff, P., … Grp, Z. S. (2011). Morbidity
among human immunodeficiency virus-exposed but
unin-fected, human immunodeficiency virus-infected, and
human immunodeficiency virus-unexposed infants in
Zimbabwe before availability of highly active antiretroviral therapy. Pediatric Infectious Disease Journal, 30(1), 45–51. doi:10.1097/INF.0b013e3181ecbf7e
Kuhn, L., Kasonde, P., Sinkala, M., Kankasa, C., Semrau, K.,
Scott, N.,… Thea, D. M. (2005). Does severity of HIV
dis-ease in HIV-infected mothers affect mortality and
morbid-ity among their uninfected infants? Clinical Infectious
Diseases, 41(11), 1654–1661.doi:10.1086/498029
Kurewa, E. N., Gumbo, F. Z., Munjoma, M. W., Mapingure, M. P., Chirenje, M. Z., Rusakaniko, S., & Stray-Pedersen, B.
(2010). Effect of maternal HIV status on infant mortality:
Evidence from a 9-month follow-up of mothers and their
infants in Zimbabwe. Journal of Perinatology, 30(2), 88–
92.doi:10.1038/jp.2009.121
Landes, M., van Lettow, M., Bedell, R., Mayuni, I., Chan, A. K., Tenthani, L., & Schouten, E. (2012). Mortality and health outcomes in HIV-infected and HIV-Uninfected mothers
at 18–20 months postpartum in Zomba District, Malawi.
PLoS ONE, 7(9),doi:10.1371/journal.pone.0044396
Lerebo, W., Callens, S., Jackson, D., Zarowsky, C., &
Temmerman, M. (2014). Identifying factors associated
with the uptake of prevention of mother to child HIV trans-mission programme in Tigray region, Ethiopia: A multilevel modeling approach. BMC Health Services Research, 14(1), 181.doi:10.1186/1472-6963-14-181
Marquez, C., Okiring, J., Chamie, G., Ruel, T. D., Achan, J.,
Kakuru, A.,… Dorsey, G. (2014). Increased morbidity in
early childhood among HIV-exposed uninfected children in Uganda is associated with breastfeeding duration.
Journal of Tropical Pediatrics, 60(6), 434. doi:10.1093/
tropej/fmu045
Mirkuzie, A. H., Sisay, M. M., Hinderaker, S. G., Moland, K.
M., & Mørkve, O. (2012). Comparing HIV prevalence
estimates from prevention of mother-to-child HIV trans-mission programme and the antenatal HIV surveillance in
Addis Ababa. BMC Public Health, 12(1), 1113. doi:10.
1186/1471-2458-12-1113
Mkwanazi, N. B., Rochat, T. J., & Bland, R. M. (2015). Living with HIV, disclosure patterns and partnerships a decade after the introduction of HIV programmes in rural South
Africa. AIDS Care – Psychological and Socio-Medical
Aspects of AIDS/HIV,doi:10.1080/09540121.2015.1028881
Moyer, C. A., Dako-Gyeke, P., & Adanu, R. M. (2013). Facility-based delivery and maternal and early neonatal mortality in sub-Saharan Africa: A regional review of the literature. African Journal of Reproductive Health, 17(3), 30–43. doi:10.2307/23485710
Mullan, Z. (2016). Transforming health care in Ethiopia. The
Lancet Global Health, 4(1), e1. doi:10.1016/S2214-109X
(15)00300-9
Nakiyingi, J. S., Bracher, M., Whitworth, J. A, Ruberantwari, A., Busingye, J., Mbulaiteye, S. M., & Zaba, B. (2003).
Child survival in relation to mother’s HIV infection and
survival: Evidence from a Ugandan cohort study. AIDS
(London, England), 17(12), 1827–1834. doi:10.1097/01.
aids.0000076274.54156.41
Naniche, D., Bardají, A., Lahuerta, M., Berenguera, A.,
Mandomando, I., Sanz, S.,… Menéndez, C. (2009).
Impact of maternal human immunodeficiency virus infec-tion on birth outcomes and infant survival in rural Mozambique. American Journal of Tropical Medicine and
Hygiene, 80(5), 870–876. doi:10.1080/09540121.2011.
579948
Ndirangu, J., Bärnighausen, T., Tanser, F., Tint, K., & Newell,
M.-L. (2009). Levels of childhood vaccination coverage and
the impact of maternal HIV status on child vaccination sta-tus in rural KwaZulu-Natal, South Africa. Tropical Medicine & International Health, 14, 1383–1393. doi:10.1111/j.1365-3156.2009.02382.x
Ndirangu, J., Newell, M.-L., Tanser, F., Herbst, A. J., & Bland,
R. (2010). Decline in early life mortality in a high HIV
prevalence rural area of South Africa: Evidence of HIV pre-vention or treatment impact? Aids (London, England), 24
(4), 593–602.doi:10.1097/QAD.0b013e328335cff5
Negash, T. G., & Ehlers, V. J. (2016). An assessment of the out-comes of prevention of mother-to-child transmission of HIV services in Addis Ababa, Ethiopia. Curationis, 39(1),
1583.doi:10.4102/curationis.v39i1.1583
Newell, M.-L. L., Coovadia, H., Cortina-Borja, M., Rollins, N., Gaillard, P., & Dabis, F. (2004). Mortality of infected and uninfected infants born to HIV-infected mothers in
Africa: A pooled analysis. The Lancet, 364(9441), 1236–
1243.doi:10.1016/S0140-6736(04)17140-7
Tura, G., Fantahun, M., & Worku, A. (2013). The effect of
health facility delivery on neonatal mortality: Systematic review and meta-analysis. BMC Pregnancy and Childbirth,
13(1), 18.doi:10.1186/1471-2393-13-18
UN DSD: Division for Sustainable Development. (2017).
United Nations Partnerships for SDGs platform.
United Nations. (2015). Countdown To Zero– Kenya. Citeseer.
Violari, A., Cotton, M. F., Gibb, D. M., Babiker, A. G., Steyn, J., Madhi, S. A.,… McIntyre, J. A. (2008). Early antiretroviral therapy and mortality among HIV-infected infants. The
New England Journal of Medicine, 359(21), 2233–2244.
WHO. (2010). PMTCT strategic vision 2010–2015: Preventing mother-to-child transmission of HIV to reach the UNGASS and millennium development goals.
WHO. (2018). Mother-to-child transmission of HIV. Retrieved
fromhttp://www.who.int/hiv/topics/mtct/about/en/
World Health Organization. (2010). Programmatic update:
Use of antiretroviral drugs for treating pregnant women and preventing HIV infection in infants. Geneva: WHO. doi:WHO/HIV/2012.6
Wudineh, F., & Damtew, B. (2016). Mother-to-child
trans-mission of HIV infection and its determinants among exposed infants on care and follow-up in Dire Dawa City, Eastern Ethiopia. AIDS Research and Treatment, 2016. doi:10.1155/2016/3262746
Zaba, B., Whitworth, J., Marston, M., Nakiyingi, J.,
Ruberantwari, A., Urassa, M.,… Crampin, A. (2005). HIV
and mortality of mothers and children. Epidemiology, 16
(3), 275–280.doi:10.1097/01.ede.0000155507.47884.43
