RESEARCH ARTICLE

Mother-to-child transmission of HIV in Kenya:

A cross-sectional analysis of the national
database over nine years
Matilu Mwau1,2*, Priska Bwana2, Lucy Kithinji2, Francis Ogollah2, Samuel Ochieng2,
Catherine Akinyi1, Maureen Adhiambo1, Fred Ogumbo1, Martin Sirengo3, Caroline Boeke4
1 Centre for Infectious and Parasitic Diseases Control Research, Kenya Medical Research Institute, Busia,
Kenya, 2 Centre for Virus Research, Kenya Medical Research Institute, Nairobi, Kenya, 3 National AIDS and
STIs Control Program, Ministry of Health, Nairobi, Kenya, 4 Clinton Health Access Initiative, Boston,
a1111111111 Massachusetts, United States of America
a1111111111
a1111111111 * [email protected]
a1111111111
a1111111111
Abstract

OPEN ACCESS Objective

Citation: Mwau M, Bwana P, Kithinji L, Ogollah F, To describe factors associated with mother-to-child HIV transmission (MTCT) in Kenya and
Ochieng S, Akinyi C, et al. (2017) Mother-to-child identify opportunities to increase testing/care coverage.
transmission of HIV in Kenya: A cross-sectional
analysis of the national database over nine years.
PLoS ONE 12(8): e0183860. https://doi.org/ Design
10.1371/journal.pone.0183860
Cross-sectional analysis of national early infant diagnosis (EID) database.
Editor: Sarah L. Pett, University of New South
Wales, AUSTRALIA
Methods
Received: February 11, 2017
365,841 Kenyan infants were tested for HIV from January 2007-July 2015 and results,
Accepted: August 11, 2017
demographics, and treatment information were entered into a national database. HIV risk
Published: August 29, 2017 factors were assessed using multivariable logistic regression.
Copyright: © 2017 Mwau et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
Results
permits unrestricted use, distribution, and 11.1% of infants tested HIV positive in 2007–2010 and 6.9% in 2014–2015. Greater odds of
reproduction in any medium, provided the original
infection were observed in females (OR: 1.08; 95% CI:1.05–1.11), older children (18–24
author and source are credited.
months vs. 6 weeks-2 months: 4.26; 95% CI:3.87–4.69), infants whose mothers received no
Data Availability Statement: All relevant data are PMTCT intervention (vs. HAART OR: 1.92; 95% CI:1.79–2.06), infants receiving no prophy-
within the paper and its Supporting Information
file.
laxis (vs. nevirapine for 6 weeks OR: 2.76; 95% CI:2.51–3.05), and infants mixed breastfed
(vs. exclusive breastfeeding OR: 1.39; 95% CI:1.30–1.49). In 2014–2015, 9.1% of infants
Funding: The authors wish to thank the Centers for
Disease Control and Prevention (CDC), USAID/
had mothers who were not on treatment during pregnancy, 9.8% were not on prophylaxis,
PEPFAR, and UNITAID for funding HIV diagnostics and 7.0% were mixed breastfed. Infants exposed to all three risky practices had a seven-
in Kenya. The IT infrastructure was funded by fold higher odds of HIV infection compared to those exposed to recommended practices.
Hewlett-Packard. None of the funders had any role
The highest yield of HIV-positive infants were found through targeted testing of symptomatic
in study design, data collection and analysis,
decision to publish, or preparation of the infants in pediatric/outpatient departments (>15%); still, most infected infants were identified
manuscript. through PMTCT programs.

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 Mother to child transmission of HIV in Kenya

Competing interests: The authors declare no Conclusion

competing interests. The IT infrastructure was
funded by Hewlett-Packard but the infrastructure Despite impressive gains in Kenya’s PMTCT program, some HIV-infected infants present
funder had no role in study design, data collection late and are not benefitting from PMTCT best practices. Efforts to identify these early and
and analysis, decision to publish, or preparation of enforce evidence-based practice for PMTCT should be scaled up. Infant testing should be
the manuscript. The infrastructure funding does
not alter our adherence to PLOS ONE policies on
expanded in pediatric/outpatient departments, given high yields in these portals.
sharing data and materials.

Introduction
Without antiretroviral therapy (ART), approximately 50% of HIV-infected infants die by the
age of two[1]. However, the use of elective caesarian section, the provision of highly active anti-
retroviral therapy (HAART) during pregnancy, and the avoidance of breastfeeding have
reduced the HIV transmission rate to less than 2% and resulted in the near elimination of
mother to child transmission (MTCT) [2, 3]. Unfortunately, barriers to healthcare and sub-
optimal infant feeding and care practices still exist in resource-limited settings and continue to
propagate transmission of HIV from mothers to infants. Identifying infected infants early and
initiating them on ART as soon as possible after diagnosis is essential to slow the progression
from HIV infection to AIDS and prolong the life of the patient[1].
Despite substantial progress in efforts to reduce MTCT of HIV in Kenya, HIV transmission
through the end of breastfeeding remains at 17%, with approximately 13,000 new HIV infec-
tions among children in 2014[4]. Option B+, an approach to prevent MTCT of HIV by offer-
ing all HIV-positive pregnant women treatment for life and ART prophylaxis to all exposed
infants, free of charge, has been scaled up through a phased rollout in Kenya starting in 2014;
by October 2015 more than 90% of all sites with programs on prevention to mother-to-child
transmission of HIV (PMTCT) or maternal, newborn, and child health had adopted it[5].
UNAIDS estimates suggest that greater than 90% of all pregnant women attending ANC in
Kenya are tested for HIV[6]. However, gaps remain. Nearly half (42%) of women do not fully
access antenatal care (at least 4 visits during pregnancy)[7], and 39% deliver outside of health-
care facilities[8]. Access to care is poorest in rural areas. Due in large part to this gap, an esti-
mated 33% of HIV-infected pregnant women are not on treatment and early infant diagnosis
of HIV (EID) testing coverage by two months of age in exposed infants was 72% in 2014[4].
Better understanding of these gaps and the remaining risk factors for HIV infection among
infants who get tested is essential to eliminate MTCT in Kenya and neighboring countries.
This study used nearly a decade of nationwide data from a national HIV laboratory data-
base of over 370,000 EID samples to assess the risk factors for HIV transmission in infants and
to identify important predictors of HIV infection over time. We also assessed which facility
entry points had the greatest yield for EID case detection of HIV-infected infants to inform
resource allocation for HIV testing. While as a registry-based study, the data have some limita-
tions, this is amongst the first studies of this scale examining risk factors for HIV infection in
infants through the period of scale-up of Option B+ in sub-Saharan Africa.

Materials and methods

Study setting and design
The EID program in Kenya is overseen by the Ministry of Health. As of 2007, there was tar-
geted testing of HIV-exposed symptomatic infants; in 2008–2009, as more resources became
available for testing, the guidelines changed to test all HIV-exposed infants. The infant HIV
testing algorithm as of 2012 in Kenya was as follows: a maternal or infant HIV antibody test

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 Mother to child transmission of HIV in Kenya

was conducted at first visit for all children of unknown HIV status aged <18 months to estab-
lish HIV exposure status. If positive, an EID test was recommended. If the EID test was posi-
tive, the infant was started on ART and if negative, the infant received an HIV antibody test at
9 months (or earlier if child developed symptoms suggestive of HIV). If the antibody test was
positive at 9 months, the infant received a confirmatory EID test. If the EID test was negative,
the HIV antibody test was repeated at 18 months or 6 weeks after cessation of breastfeeding in
a child >18 months[9]. EID testing coverage by 2 months of age in HIV-exposed infants in
Kenya was estimated to be below 50% in 2011 and increased to 72% in 2014[4]. In 2015, the
algorithm was updated to recommend an EID test at 6 weeks or first contact after 6 weeks[10].
Seven laboratories form the testing network and laboratory request forms are compiled into a
national database across the laboratories. Thus, the database covers nearly all infants receiving
EID testing in the country. Data from the database can be viewed on a national dashboard
(http://eid.nascop.org/). Mean turnaround time from sample collection to results dispatch
from the laboratory has changed over time but was 17 days as of July 2015[11]. This cross-sec-
tional analysis was based on a retrospective review of all data stored in the national HIV data-
base between January 2007 and July 2015.

Clinical and laboratory procedures

Dried Blood Spots (DBS) were collected as part of routine care for infants with suspected or
known HIV exposure as previously described[12]. Briefly, samples were collected under sterile
conditions from infants using either a heel prick or finger prick depending on the age and
weight of the infant. Sample collection occurred at several entry points including maternal and
child health (MCH)/PMTCT clinics, the comprehensive clinic care (CCC)/patient support
center (PSC), the outpatient department (OPD), and the pediatric ward. DBS filter papers
were labeled and dried separately on a drying rack overnight. They were then packaged using
glycine envelopes and sealed plastic bags under sterile conditions and sent to the testing labo-
ratory by a courier system accompanied by a laboratory request form.
CobasAmpliPrep/CobasTaqMan_HIV-1 Qual or Abbot real-time HIV automated PCR
test procedures were conducted on each sample based on the manufacturer’s guidelines, as
described previously[12–14]. The CobasAmpliPrep/CobasTaqMan_HIV-1 Qual uses one
dried blood spot (70uL) while the Abbot real-time HIV automated PCR testing uses two spots
(140uL) of blood for the test. All positive samples were retested to confirm their status while a
request for recollection of a new sample was made in cases where the test failed or number of
blood spots was not sufficient to allow repeat confirmatory testing for positive samples.
Lab results were stored in an online accessible Laboratory Information System database
provided by the Ministry of Health, along with the laboratory request form indicating the
number of samples sent to the testing laboratory, the age and sex of the infant, mother’s HIV
status, breastfeeding status, point of entry, medication given to the mother, and prophylaxis
given to the baby. The database was retrospectively accessed to extract the relevant data and
run these analyses.

Study population
A total of 370,196 samples were successfully collected from infants visiting health facilities
across all regions in Kenya between January 2007 and July 2015 and tested in seven national
laboratories. 362 samples had the same patient ID number, came from the same facility, were
tested on the same date, and were from an individual of the same age and sex as another sam-
ple; these were considered to be duplicate tests from the same infant and were excluded from
the dataset. Due to improper DBS sample collection, packaging or labeling, 3228 samples were

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 Mother to child transmission of HIV in Kenya

rejected and were therefore excluded from the analysis. Patients with age listed as a negative
value or greater than or equal to 2 years (n = 765) were excluded from the main analysis; a sec-
ondary analysis was conducted setting age to missing in these individuals. Patients with miss-
ing data on other predictor variables were included in a missing indicator category. 365,841
patients had a valid test result and were included in the tables and primary analyses.

Statistical analysis
Demographic data were summarized with descriptive statistics. The primary outcome was
infant HIV status (infected vs. uninfected). We examined predictors of infant HIV status,
including breastfeeding, age, prophylaxis, antiretroviral therapy and portal of entry. As a pre-
liminary statistical analysis, continuous predictors were compared in relation to infant HIV
result using Student’s T-tests if normally distributed or Mann-Whitney U tests if skewed. Cate-
gorical data were compared using the Fisher’s exact test or the chi square test.
Logistic regression was used to calculate univariate odds ratios of potential predictors in
relation to infant HIV result and 95% confidence intervals. Variables that were significantly
associated with infant HIV infection in univariate models were included in a multivariate
logistic regression model. Finally, we combined all behavioral risk factors identified for infant
HIV infection into one variable and assessed the increased odds of infection in an infant with
multiple risk factors. The models accounted for clustering by health facilities using the vce
(cluster) function for statistical analysis. Reference groups were selected based on the most
common group and/or the standard of care in Kenya. The interaction between age and sex
was examined and a Wald p-value for interaction was calculated. Separate logistic regression
models were run by time period (2007–2010, prior to any Option B+ programs and when EID
testing was limited and targeted; 2011–2013, when EID testing was scaled up and Option B+
was piloted at some sites; and 2014–2015, when Option B+ was rolled out nationally and EID
coverage continued to expand) to assess differences over time as Kenya’s national testing and
treatment program grew and developed. Significance levels were set at p<0.05. All analysis in
this study was conducted using Stata Version 13 (StataCorp LP, College Station, Texas, USA).

Quality assurance
Kenya has a national quality assurance program for the seven molecular laboratories. The pro-
gram supports external quality assurance, training/registration of users, and harmonisation of
operating procedures. All seven labs are enrolled and participate in the CDC Atlanta profi-
ciency testing program. They also participate in a quarterly inter-laboratory EQA programme.

Ethical approval
This study was approved by the Scientific Steering Committee and Ethical Review Committee
of the Kenya Medical Research Institute (Protocol SSC No. 1066). The need for participant
consent was waived. No identifiable patient information was included in the database, but
facility-specific patient identification numbers were included. NASCOP considers the EID ser-
vice as a national HIV program and a standard of care.

Results
Patient characteristics and univariate and multivariate logistic regression analyses are pre-
sented in Table 1. Of the 365,841 infants in the dataset, 8.9% (32,441) were found to be HIV-
infected. 50.4% of samples (of those with known sex) were from females. Data on sex was
unavailable for 10.9% of samples. The median age at testing was 1.8 months (IQR: 1.5–5.0

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 Mother to child transmission of HIV in Kenya

Table 1. Predictive factors for HIV positivity in 365,841 infants testing for HIV in Kenya.
Factor Univariate Multivariate
N % HIV+ OR 95%CI OR 95%CI
Gender Male 161,682 8.4% Ref Ref
Female 164,259 8.9% 1.06 1.04– 1.08 1.05–
1.09 1.11
Missing 39,900 10.4% 1.26 1.19– 1.11 1.03–
1.32 1.20
Age group 0–6 weeks 47,968 10.1% 2.43 2.25– 1.72 1.59–
2.63 1.86
6 weeks-2 months 138,494 4.4% Ref Ref
2–6 months 86,877 9.4% 2.25 2.12– 1.76 1.68–
2.39 1.86
6–9 months 35,888 11.9% 2.93 2.73– 2.08 1.95–
3.13 2.22
9–18 months 46,834 16.3% 4.23 3.96– 3.05 2.89–
4.51 3.21
18–24 months 4,599 21.6% 5.98 5.36– 4.26 3.87–
6.67 4.69
Missing 5,181 8.3% 1.96 1.73– 1.47 1.26–
2.22 1.72
PMTCT AZT from 14 weeks of pregnancy or later; AZT+3TC+sdNVP during labor; AZT 41,394 6.5% 1.13 1.06– 1.13 1.06–
Intervention +3TC for 7 days postpartum 1.21 1.20
HAART 125,166 5.8% Ref Ref
Interrupted HAART (HAART until end of breastfeeding) 11,437 7.0% 1.22 1.09– 1.20 1.08–
1.37 1.33
None 43,837 15.2% 2.90 2.67– 1.92 1.79–
3.16 2.06
Other 12,711 8.6% 1.53 1.37– 1.23 1.10–
1.72 1.36
Single dose NVP Only 8,633 9.1% 1.62 1.45– 1.32 1.20–
1.80 1.45
Missing 122,663 10.7% 1.94 1.80– 1.53 1.43–
2.10 1.63
Infant Prophylaxis AZT+3TC for 7 days only 128 2.3% 0.57 0.17– 0.40 0.12–
1.90 1.35
NVP during breastfeeding 50,505 6.3% 1.58 1.45– 1.30 1.20–
1.73 1.41
NVP for 6 weeks (Mother on HAART or not breastfeeding) 67,429 4.0% Ref Ref
None 19,889 21.7% 6.56 5.83– 2.76 2.51–
7.39 3.05
Other 5,689 8.4% 2.18 1.82– 1.46 1.25–
2.60 1.70
Single dose NVP+AZT+3TC 3,436 8.1% 2.09 1.74– 1.45 1.22–
2.50 1.73
Single dose NVP Only 21,541 5.9% 1.49 1.34– 1.19 1.09–
1.65 1.30
Missing 197,224 10.2% 2.71 2.48– 1.56 1.43–
2.95 1.70
Breastfeeding Exclusive breastfeeding 167,166 6.2% Ref Ref
Mixed breastfeeding 23,682 15.2% 2.73 2.48– 1.39 1.30–
3.00 1.49
Breastfeeding, unspecified 32,609 11.3% 1.94 1.81– 1.13 1.05–
2.08 1.20
(Continued)

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 Mother to child transmission of HIV in Kenya

Table 1. (Continued)

Factor Univariate Multivariate

N % HIV+ OR 95%CI OR 95%CI
No breastfeeding 37,856 9.7% 1.63 1.49– 0.95 0.88–
1.80 1.02
Missing 104,528 10.6% 1.81 1.70– 0.98 0.92–
1.92 1.04
Entry point Comprehensive clinic care/patient support center 54,257 9.1% 1.27 1.17– 1.10 1.03–
1.38 1.17
Maternal and child health/PMTCT 208,834 7.3% Ref Ref
Maternity 2,505 9.0% 1.26 1.05– 1.12 0.94–
1.51 1.33
Outpatient department 10,216 18.7% 2.93 2.68– 1.65 1.52–
3.19 1.79
Other 9,753 12.6% 1.83 1.64– 1.15 1.03–
2.05 1.28
Pediatric Ward 3,381 32.9% 6.23 5.26– 3.32 2.82–
7.39 3.92
Missing 76,895 10.2% 1.44 1.34– 0.92 0.87–
1.55 0.99
Test year 2007 1,548 31.5% 6.61 5.90– 3.72 2.85–
7.41 4.85
2008 18,257 10.1% 1.62 1.52– 1.00 0.89–
1.72 1.13
2009 19,116 11.7% 1.91 1.81– 1.37 1.21–
2.03 1.54
2010 57,584 10.7% 1.72 1.65– 1.12 1.03–
1.81 1.22
2011 58,213 10.0% 1.61 1.53– 1.08 0.99–
1.69 1.18
2012 55,063 8.2% 1.29 1.23– 0.91 0.86–
1.36 0.97
2013 55,070 8.0% 1.25 1.19– 0.99 0.94–
1.31 1.06
2014 58,495 7.1% 1.10 1.05– 0.96 0.91–
1.16 1.02
2015 42,495 6.5% Ref Ref

Univariate and multivariable logistic regression accounting for clustering by health facility. The multivariable model was adjusted for all factors in this table.
The missing indicator method was used to account for missing data. Abbreviations: AZT: zidovudine. 3TC: lamivudine. Sd: single dose. NVP: nevirapine.
HAART: highly active antiretroviral therapy. PMTCT: prevention of mother-to-child transmission of HIV.

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months). Age at testing did not differ substantially between the sexes. 51.5% mothers were
confirmed to be on highly active antiretroviral therapy (HAART; out of those with data on
treatment regimen) and an additional 4.7% on interrupted HAART. 18.0% were on no treat-
ment. 11.8% of infants were not on any HIV prophylaxis (among those with known prophylaxis
status). Exclusive breastfeeding (EBF) was provided to 64.0% of infants (out of those with
breastfeeding information), while 14.5% of infants were not breastfed. Mixed breastfeeding was
practiced by 9.1% of infants, although only 60.4% of those infants were under 6 months of age
and it is unknown whether the older children were previously exclusively breastfed and cur-
rently complementary feeding or were previously mixed breastfed. In addition, mixed breast-
feeding decreased over time. 12.5% of infants were breastfed but did not have information
on whether it was exclusive or mixed (hereafter referred to as “unspecified breastfeeding”).

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 Mother to child transmission of HIV in Kenya

Approximately 72.3% of samples were collected via PMTCT/maternal and child health (MCH)
clinic samples, while 18.8% were collected from CCC/ PSC, 3.5% from OPD, 1.2% from the
pediatric ward and 0.9% from the maternity ward. The vast majority of samples across entry
points were from patients ages 1 to 2 months, although the entry points with the most extreme
peak in that age range were from PMTCT/MCH and CCC/PSC.
In multivariate analyses, the odds ratio for HIV infection in females was 1.08 (95% CI 1.05–
1.11) compared to males. When examining the sex differences in infection by age, there was a
statistically significant difference between positivity in females and males through 6 months
but no statistically significant difference in older children (p-value for interaction = 0.01).
10.1% of newborns less than 6 weeks of age were found to be infected with HIV. Compared to
infants being tested at 6 weeks to 2 months (the majority of infants), the odds ratio of testing
positive for HIV infection was 1.72 (95% CI: 1.59–1.86) in infants aged 0 to 6 weeks. However,
most of those infants were listed as testing at 0 months, which may have represented a data
entry error; sensitivity analyses in which these infants were considered to be missing age
showed an attenuated association in this age group [OR changed to 1.28 (95% CI: 1.18–1.40)].
The percentage testing positive for infection was the lowest at 6 weeks to 2 months when the
largest number of infants were tested, and then increased with age to 21.6% at 18 months to 2
years (76.3% of infants in this category were 18.0–18.5 months old). Compared to infants
being tested at 6 weeks to 2 months, the odds ratio of testing positive for HIV infection was
1.76 (95% CI: 1.68–1.86) in infants 2 to 6 months, increasing to 4.26 (95% CI: 3.87–4.69) in
infants 18–24 months. Infants whose mothers were not taking ART had nearly double the
odds of the HIV infection when compared to those whose mothers were on treatment (multi-
variable-adjusted OR 1.92; 95% CI 1.79–2.06). For infants not on any prophylaxis, the odds
ratio for HIV infection was 2.76 (95% CI 2.51–3.05) when compared to those who were on
nevirapine (NVP) for six weeks whose mothers were on ART or were not breastfeeding. The
percentage of infants on nevirapine for 6 weeks that tested positive was 4.0% vs. 21.7% of
infants on no prophylaxis. Among infants whose mothers were on HAART, the differences in
HIV infection by infant prophylaxis regimen were smaller but still substantial; 3.3% for those
on nevirapine for 6 weeks and mother breastfeeding while 11.8% for those on no prophylaxis.
Infants who were categorized as mixed breastfed had 1.39 (95% CI: 1.30–1.49) times the odds
of HIV infection when compared to exclusively breastfed infants. There was not a statistically
significant difference in HIV infection between exclusively breastfeeding and not breastfeed-
ing. The highest yield for detecting infected patients was observed in the pediatric ward and
the outpatient department. For infants who sought health services at the pediatric ward,
the odds ratio of HIV infection was 3.32 (95% CI 2.82–3.92), while for those seen at the outpa-
tient departments the odds ratio was 1.65 (95% CI 1.52–1.79) when compared to the MCH-
PMTCT. However, given the difference in the volume of patients tested in each entry point,
only 3.4% (5.3% in 2014–2015) of the HIV-infected infants were identified via the pediatric
ward and 5.9% (9.0% in 2014–2015) through the outpatient department, whereas 46.9%
(55.8% in 2014–2015) of patients were identified through MCH/PMTCT.
In a model combining sub-optimal behaviors for HIV transmission, the adjusted odds ratio
of HIV infection for infants who did not receive infant prophylaxis, were mixed fed, and
whose mothers did not receive any form of antiretroviral therapy (N = 2,550) was 7.10 (95%CI
5.64–8.93) compared to infants who received nevirapine for 6 weeks, were not breastfed, and
whose mothers were on HAART (N = 3,325), and the odds were similar when compared to
infants who received nevirapine, were exclusively breastfed, and mothers were on HAART
[OR: 6.91 (95% CI: 6.14–7.78); S1 Table].
Table 2 shows multivariable-adjusted model results stratified by early and recent time
period. The percentage of infants receiving an EID test who tested positive for HIV infection

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 Mother to child transmission of HIV in Kenya

Table 2. Risk factors for HIV positivity in 2007–2010 (N = 96,505; 11.1% HIV-positive) vs. 2011–2013 (N = 168,346; 8.8% HIV-positive) vs. 2014–2015
(N = 100,990; 6.9% HIV-positive) among infants testing for HIV in Kenya.
Factor 2007–2010 2011–2013 2014–2015
N % HIV OR 95%CI N % HIV OR 95%CI N % HIV OR 95%CI
+ + +
Gender Male 37,305 10.8% Ref 77,365 8.4% Ref 47,012 6.7% Ref
Female 37,639 11.4% 1.07 1.03– 78,483 9.0% 1.09 1.05– 48,137 6.9% 1.08 1.02–
1.12 1.13 1.14
Age group 0–6 weeks 23,035 11.2% 1.50 1.31– 17,115 9.9% 1.76 1.54– 7,818 7.2% 1.79 1.59–
1.71 2.01 2.03
6 weeks-2 months 23,039 6.8% Ref 63,735 4.6% Ref 51,720 3.1% Ref
2–6 months 24,858 11.1% 1.57 1.42– 39,968 9.2% 1.71 1.60– 22,051 7.9% 2.05 1.88–
1.72 1.82 2.23
6–9 months 11,959 13.6% 2.02 1.82– 17,094 11.1% 1.89 1.75– 6,835 11.0% 2.21 1.98–
2.24 2.04 2.46
9–18 months 11,455 16.6% 2.55 2.25– 25,273 15.3% 2.76 2.58– 10,106 18.5% 4.05 3.64–
2.89 2.96 4.50
18–24 months 982 20.6% 3.37 2.70– 2,632 19.3% 3.60 3.17– 985 28.7% 7.02 5.81–
4.20 4.08 8.49
PMTCT AZT from 14 weeks of pregnancy or 8,559 8.7% 1.06 0.95– 23,819 6.0% 1.15 1.05– 9,016 5.8% 1.22 1.07–
Intervention later; AZT+3TC+sdNVP during labor; 1.18 1.26 1.39
AZT+3TC for 7 days postpartum
HAART 21,979 9.1% Ref 49,017 5.9% Ref 54,170 4.4% Ref
Interrupted HAART (HAART until end 805 10.2% 0.90 0.71– 6,691 6.9% 1.24 1.09– 3,941 6.5% 1.25 1.06–
of breastfeeding) 1.14 1.41 1.48
None 15,254 12.0% 1.44 1.29– 21,448 14.8% 2.06 1.86– 7,135 23.3% 2.40 2.16–
1.61 2.28 2.67
Other 1,042 13.0% 1.24 1.01– 8,428 8.2% 1.19 1.04– 3,241 8.4% 1.46 1.25–
1.52 1.37 1.71
Single dose NVP Only 3,100 10.1% 1.22 1.04– 4,307 9.0% 1.50 1.31– 1,226 6.9% 1.20 0.93–
1.43 1.71 1.56
Infant AZT+3TC for 7 days only 0 - - 25 0.0% - - 103 2.9% 0.47 0.13–
Prophylaxis 1.68

NVP during breastfeeding 20 5.0% 0.59 0.03– 28,385 6.5% 1.26 1.14– 22,100 6.0% 1.26 1.13–
10.16 1.39 1.40
NVP for 6 weeks (Mother on HAART or 13 7.7% Ref 27,478 4.4% Ref 39,938 3.8% Ref
not breastfeeding)
None 35 11.4% 1.23 0.16– 11,731 20.8% 2.57 2.29– 8,123 23.0% 2.30 2.04–
9.34 2.89 2.58
Other 6 16.7% 1.52 0.08– 2,567 10.4% 1.51 1.22– 3,116 6.8% 1.28 1.04–
30.12 1.87 1.57
Single dose NVP+AZT+3TC 36 0.0% - - 2,349 6.8% 1.19 0.97– 1,051 11.2% 2.05 1.55–
1.45 2.71
Single dose NVP Only 19 0.0% - - 13,256 6.4% 1.23 1.10– 8,266 5.0% 1.05 0.92–
1.37 1.20
Breastfeeding Exclusive breastfeeding 13,199 12.4% Ref 83,080 6.5% Ref 70,887 4.7% Ref
Mixed breastfeeding 5,112 9.7% 0.74 0.65– 12,330 14.6% 1.39 1.27– 6,240 21.1% 1.84 1.67–
0.83 1.52 2.03
Breastfeeding, unspecified 18,491 10.3% 0.79 0.71– 9,832 13.0% 1.25 1.13– 4,286 12.2% 1.17 1.03–
0.89 1.37 1.33
No breastfeeding 11,134 9.4% 0.66 0.59– 19,213 9.9% 1.02 0.93– 7,509 9.8% 1.03 0.88–
0.74 1.12 1.20
Entry point Comprehensive clinic care/patient 11,539 12.7% 1.22 1.12– 26,043 8.9% 1.03 0.94– 16,675 6.9% 1.01 0.91–
support center 1.32 1.13 1.11
(Continued)

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 Mother to child transmission of HIV in Kenya

Table 2. (Continued)

Factor 2007–2010 2011–2013 2014–2015

N % HIV OR 95%CI N % HIV OR 95%CI N % HIV OR 95%CI
+ + +
Maternal and child health/PMTCT 45,312 9.8% Ref 93,876 7.4% Ref 69,646 5.5% Ref
Maternity 534 11.4% 1.19 0.82– 1,191 9.2% 1.07 0.86– 780 7.2% 0.96 0.71–
1.72 1.33 1.30
Outpatient department 1,210 15.4% 1.44 1.18– 6,537 16.9% 1.55 1.38– 2,469 25.2% 1.81 1.60–
1.75 1.73 2.04
Other 4,444 11.3% 1.09 0.96– 3,753 14.8% 1.40 1.19– 1,556 10.7% 0.79 0.58–
1.24 1.66 1.08
Pediatric Ward 1,128 26.1% 2.63 2.09– 1,337 33.7% 3.53 2.86– 916 40.1% 3.90 3.08–
3.32 4.35 4.93

Multivariable logistic regression accounting for clustering by health facility. A separate model was run for each time period. The multivariable model was
adjusted for all factors in this table plus test year. The missing indicator method was used to account for missing data; to save space, missing categories are
not shown. Abbreviations: AZT: zidovudine. 3TC: lamivudine. Sd: single dose. NVP: nevirapine. HAART: highly active antiretroviral therapy. PMTCT:
prevention of mother-to-child transmission of HIV

https://doi.org/10.1371/journal.pone.0183860.t002

decreased over time; in 2007–2010, positivity was 11.1% while in 2014–2015, positivity was
6.9%. Most associations were consistent over time, although some associations varied in their
strength.
The proportion of mothers not on ART during pregnancy (among those with treatment
data) decreased dramatically over time, from 30.1% in 2007–2010 to 9.1% in 2014–2015. The
percentage of infants born to mothers on HAART who were HIV-infected decreased from
9.1% in 2007–2010 to 4.4% in 2014–2015. Infant prophylaxis was not widely available in 2007–
2010 so data was not routinely collected, but between 2011–2013 and 2014–2015 the propor-
tion of infants receiving no prophylaxis decreased from 13.7% to 9.8%.
The higher prevalence of HIV infection among older children compared to younger chil-
dren was stronger after scale-up of Option B+ (adjusted OR comparing children aged 18–24
months to children 6 weeks to 2 months in 2014–2015: 7.02; 95% CI: 5.81–8.49).
Mixed breastfeeding decreased from 10.7% of infants in 2007–2010 (plus 38.6% unspecified
breastfeeding) to 7.0% (plus 4.8% unspecified breastfeeding) in 2014–2015. There may have
been differences in the way that the breastfeeding categories were defined/reported over the
years, as in 2007–2010”mixed breastfeeding” appeared to be protective compared to exclusive
breastfeeding whereas in more recent years it was harmful. Not breastfeeding appeared protec-
tive compared to exclusive breastfeeding in 2007–2010 (OR: 0.66; 95% CI: 0.59–0.74) while
there was no association in 2014–2015. Finally, associations between entry point and HIV
have changed over time, particularly in that the pediatric ward in more recent years had an
extremely high yield for identifying infected patients.
There were no substantial differences in the study findings when patients with age listed as
a negative value or greater than or equal to 2 years were included in the analysis with age listed
as missing.

Discussion
For this study, we analysed a comprehensive national dataset from Kenya covering nearly a
decade to describe the determinants of HIV status in infants below 2 years of age at testing.
We observed greater odds of HIV infection in females, older children, infants whose mothers
received no PMTCT intervention, infants receiving no HIV prophylaxis, and infants who were

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 Mother to child transmission of HIV in Kenya

mixed breastfed. Exposure to risky practices (mother not on HAART, no infant prophylaxis,
mixed breastfeeding) was associated with a seven-fold higher odds of HIV-positivity compared
to exposure to recommended practices (mother on HAART, infant on nevirapine for six
weeks, no breastfeeding). With PMTCT/EID program growth and more patients in care, there
has been a decrease in risky practices over time, but even the recent data suggests that some
infants are not reached in time for prevention; these findings would likely be more striking in
other countries in sub-Saharan Africa where PMTCT programs are not as strong. Finally, the
pediatric ward and outpatient department had the highest testing yield across entry portals,
but most HIV-infected infants were identified through PMTCT/MCH programs.
Most importantly, many infants were not identified as infected until older ages and received
sub-optimal prevention practices (lack of HAART for mother, infant prophylaxis, exclusive
breastfeeding or exclusive replacement feeding). Option B+ has been scaled up in recent years
and the number of new pediatric infections in Kenya has decreased by 29% from 2009 to 2014
[4]. Yet hundreds to thousands of infants are still becoming infected each year because their
mothers are not enrolled in care. Barriers to testing and care include distance to health facility
and transportation costs, facility inefficiencies, such as stock-outs and long wait times, and per-
sistent shamefulness and stigma[15]. Expanded testing efforts in adolescent and early adult
women and increased HIV self-testing availability may help to expand case-finding in women
of childbearing age.[16] Many pregnant women do not come to health facilities for antenatal
care until late in pregnancy[17] if at all; a high proportion of women deliver outside of facili-
ties. HIV-infected women who deliver outside of facilities tend to have lower income and be
less educated and less likely to be on treatment[18], meaning that their infants are at especially
high risk. Pilot interventions that have been shown to improve PMTCT program coverage,
retention, and quality include mHealth tools[19] such as SMS[20], rapid results initiatives[21],
systems engineering approaches[22], and efforts to reduce health provider absenteeism[23];
these could be considered in areas struggling with program performance. In addition, there
likely remain inconsistencies with health provider care among women and infants enrolled in
PMTCT programs. A case-control study in Western Kenya observed that Infants were more
likely to be infected with HIV if their provider did not follow maternal and infant ART guide-
lines[24]. Ensuring reinforcement of guidelines through periodic re-trainings and supportive
supervision, as well as strong supply chain management systems will be important to continue
to strengthen the PMTCT program.
We observed HIV infections in some infants despite their mothers being on HAART; the
percentage of infected infants in this category declined over time as drug regimens changed to
4.4% in 2014–2015. Possible reasons for transmission in these infants include late treatment
initiation in mothers, treatment nonadherence, lower efficacy on certain treatments, drug
resistance, and stock-outs. This database does not contain information on these factors and
therefore we are only able to speculate on the relative contribution of each one. Some mothers
had interrupted HAART, indicating that non-adherence to treatment may be another barrier
to care and testing. Strong adherence support programs are also important to minimize trans-
mission during pregnancy. Innovative methods including community adherence groups[25]
and transport reimbursement for low-income patients[26] may help to improve drug adher-
ence and retention in PMTCT programs. New treatment regimens for mothers and prophy-
laxis options for infants will likely influence transmission rates in the future.
Thousands of infants are still exposed to the sub-optimal practice of mixed breastfeeding
each year in Kenya, and these infants had worse outcomes compared to exclusively breastfed
infants and infants not given any breastmilk. The dangers posed by mixed feeding have been
well-described in the literature[27–31]. Besides pointing to a gap in program coverage, these
findings illustrate a need for enhanced education of the public that this practice is detrimental.

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 Mother to child transmission of HIV in Kenya

The Kenyan National Demographic and Health Survey noted that by 2014 exclusive breast-
feeding had increased to 61% in infants less than 6 months, a near doubling from 32% in 2009
[32]. Yet a recent study among women in Nairobi found that fear of stigma and discrimination
around HIV was a persistent barrier to exclusive breastfeeding[33]. In this study, authors con-
cluded that health education and counseling as well as male partner support helped to mitigate
these issues. Other studies have shown that intensive counseling is a viable way to increase
EBF in resource-limited settings[34], although in an intervention study in Nairobi, breastfeed-
ing counseling alone did not increase EBF[35]. Regardless, there is more work to be done to
reduce mixed breastfeeding in infants younger than 6 months.
In this study we found that HIV positivity did not differ significantly between EBF and
exclusive replacement feeding (ERF) after adjustment for other factors, even when adjusted for
age. This was surprising, as exclusive replacement feeding should significantly reduce HIV
transmission. It is possible that due to stigma, or the costs associated with ERF, some of those
who said they provided replacement feeding for their infants also breastfed from time to time,
leading to some measurement error in this category.
Infants who entered care and treatment through outpatient departments or the pediatric
wards were more likely to be HIV-infected than those entering through any other service
point. This finding is not surprising, as those infants come to hospital due to illnesses which
may include, or could be related to, HIV, and supports the latest Kenyan guidelines stating
that all children presenting for care should be offered an HIV test[36]. In addition, testing in
these infants was likely offered in a targeted fashion; for example, symptomatic infants were
more likely to be tested. The high proportion of infected patients suggests that these entry
points may be important for expanded infant testing to identify more HIV-exposed infants
that are not reached by routine testing through PMTCT programs. In the future, EID detection
efforts could be expanded further to better cover patients in alternative entry points such as
OPD and pediatric wards to identify those who are missed by PMTCT testing programs, given
the high yield in these areas. This is in line with current WHO recommendations, which state
that in settings with generalized epidemics, HIV testing should be performed on infants with
unknown HIV status who are admitted to inpatient and nutrition wards and offered to infants
with unknown HIV status at outpatient and immunization clinics[37]. Increased resources for
testing at these portals may be important. However, it is important to note that the greatest
numbers of cases are still detected through MCH/PMTCT programs, despite the lower yields
in these portals, and these programs should continue this important work. Of note, a number
of studies on improving Kenya’s EID program are recently completed or still ongoing[38–41].
Through continued national monitoring efforts in Kenya and scaling up such efforts in other
countries, we can continue to work to minimize transmission of HIV to infants.
Overall, we observed slightly higher odds of positivity in female infants compared to male
infants from birth to six weeks. While this small difference could be due to chance, this phe-
nomenon has been described previously and there are theories that female infants may be
more susceptible to HIV infection in the in-utero and peripartum period [42–44]. While the
exact mechanism is not known, hypotheses include chromosomal affinity and a higher rate of
male intrauterine death among HIV-infected fetuses, leading to females being more likely to
be HIV infected at birth. In this database, females did not appear to be testing later than males,
so age at testing did not seem to explain the imbalance. Confirmation in other studies and fur-
ther investigation is needed to better understand this phenomenon.
This study has a number of limitations. Firstly, it is observational and cross-sectional; thus,
causal relationships cannot be inferred. We did not have access to data on all predictors of
infant HIV transmission and all potential confounders. In addition, the study data come from
a national health registry system and were not collected for the purpose of a research study;

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 Mother to child transmission of HIV in Kenya

thus, there were large amounts of missing data for some indicators and some inaccuracies are
possible. Along those lines, given the vagueness of the patient identification numbers at some
facilities, we were unable to assess tests from the same individuals or calculate a seroconversion
rate among patients with multiple tests. Strengthening patient identification systems and data
entry would further maximize the utility of this database. This analysis did not include out-
come data on HIV-infected infants following diagnosis; linkage to care and retention in care
for these infants is an important area for future research. Finally, the data is based on infants
who were tested for HIV, which, while covering >70% of exposed infants, does not include the
infants outside of care who are at highest risk of HIV transmission. This also means that com-
parisons between groups cannot be interpreted as nationally representative, do not necessarily
represent transmission, and are in part a product of testing coverage. The strengths of this
study include its large size, numerous risk factors examined, and comprehensiveness across
Kenya over nearly a decade.

Conclusions
This study emphasizes the importance of national health registry systems to monitor the suc-
cess of programs such as Option B+ and to inform testing for EID. Given the relative success
of Kenya’s national program, the associations are likely to be even more striking in other coun-
tries in sub-Saharan Africa with less successful PMTCT programs. We have confirmed risk
factors previously seen on a smaller scale in this national dataset, and illustrated the impact of
exposure to multiple risk factors overall and over time. The findings point to a need for
resources to continue to reinforce best treatment and prophylaxis prescribing behavior, pro-
mote exclusive breastfeeding, and test infants early in life and at testing portals with greater
case-finding. Routine point of care testing will be important to dramatically reduce time to
treatment initiation for HIV-infected infants. Most importantly, efforts must continue to
reach patients that are not coming for PMTCT programs.

Supporting information
S1 Table. Sub-optimal behaviors in relation to HIV positivity in 365,841 infants testing for
HIV in Kenya. Univariate and multivariate logistic regression accounting for clustering by
health facility. The multivariable model was adjusted for sex, age, entry point, and year. The
missing indicator method was used to account for missing data. Abbreviations: NVP: nevira-
pine. HAART: highly active antiretroviral therapy. PMTCT: prevention of mother-to-child
transmission of HIV.
(DOCX)

Acknowledgments
The authors wish to thank the Centers for Disease Control and Prevention (CDC), USAID/
PEPFAR, and UNITAID for funding HIV diagnostics in Kenya, as well as the Clinton Health
Access Initiative for technical support.

Author Contributions
Conceptualization: Matilu Mwau, Martin Sirengo.
Data curation: Matilu Mwau, Priska Bwana, Lucy Kithinji, Francis Ogollah, Samuel Ochieng,
Catherine Akinyi, Maureen Adhiambo, Fred Ogumbo.
Formal analysis: Matilu Mwau, Lucy Kithinji, Caroline Boeke.

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 Mother to child transmission of HIV in Kenya

Funding acquisition: Matilu Mwau.

Investigation: Matilu Mwau.
Methodology: Matilu Mwau, Samuel Ochieng, Catherine Akinyi, Maureen Adhiambo, Fred
Ogumbo.
Project administration: Matilu Mwau, Lucy Kithinji.
Resources: Matilu Mwau.
Software: Matilu Mwau.
Supervision: Matilu Mwau.
Validation: Matilu Mwau.
Visualization: Matilu Mwau.
Writing – original draft: Matilu Mwau, Priska Bwana, Caroline Boeke.
Writing – review & editing: Matilu Mwau, Priska Bwana, Francis Ogollah, Samuel Ochieng,
Catherine Akinyi, Maureen Adhiambo, Martin Sirengo, Caroline Boeke.

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