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Review nature publishing group

Seeking wider access to HIV testing for adolescents in


sub-Saharan Africa
Nadia A. Sam-Agudu1,2,3,4, Morenike O. Folayan5 and Echezona E. Ezeanolue6,7

More than 80% of the HIV-infected adolescents live in sub- in sub-Saharan Africa, early detection and treatment as well as
Saharan Africa. Acquired immune deficiency syndrome (AIDS)- the prevention of new infections are important. With respect to
related mortality has increased among adolescents 10–19 y new infections, female adolescents are of particular concern. In
old. The impact is highest in sub-Saharan Africa, where >80% of 2013, approximately 65% of all new adolescent HIV infections
HIV-infected adolescents live. The World Health Organization has were among girls, largely in sub-Saharan African countries
cited inadequate access to HIV testing and counseling (HTC) as (3,6). Of the 1.7 million African ALHIV, an estimated 1 million
a contributing factor to AIDS-related adolescent deaths, most of (nearly 60%), are female (7). In countries such as South Africa,
which occur in sub-Saharan Africa. This review focuses on stud- Sierra Leone and Gabon, girls represent more than 80% of new
ies conducted in high adolescent HIV-burden countries targeted HIV infections in adolescents (4,8). Regardless of gender, the
by the “All In to End Adolescent AIDS” initiative, and describes vast majority of African adolescents, including those already
barriers to adolescent HTC uptake and coverage. Fear of stigma infected with HIV, do not know their HIV status (3,6). The
and family reaction, fear of the impact of a positive diagnosis, rates of HIV testing among adolescents range from a low of 1%
perceived risk with respect to sexual exposure, poor attitudes in Congolese males to 44% in Malawian females, with a 16.4%
of healthcare providers, and parental consent requirements are average testing rate between 18 high-burden African coun-
identified as major impediments. Most-at-risk adolescents for tries (8). Limited access to HIV testing and counseling (HTC),
HIV infection and missed opportunities for testing include, those leading to late or limited access to quality care have been cited
perinatally infected, those with early sexual debut, high mobil- by the World Health Organization (WHO) and UNAIDS as a
ity and multiple/older partners, and pregnant and nonpregnant causative factor in the increase in ALHIV mortality over the
females. Regional analyses show relatively low adolescent test- past decade (6,9). Therefore, low rates of testing, especially in
ing rates and more restrictive consent requirements for HTC in the highest adolescent HIV-burden countries should be evalu-
West and Central Africa as compared to East and southern Africa. ated, and barriers to wider access to testing-and therefore to
Actionable recommendations for widening adolescent access to early treatment and treatment-as-prevention- should be effec-
HTC and therefore timely care include minimizing legal consent tively addressed.
barriers, healthcare provider training, parental education and In February 2015, the United Nations launched the “All-In”
involvement, and expanding testing beyond healthcare facilities. initiative to end Adolescent AIDs, which aims to reduce new
adolescent infections by 75%, to reduce AIDS-related mor-
tality by 65%, and to achieve zero discrimination by 2020 (8).

A dolescents 10–19 y old have recently received increased


global focus for targeted HIV research and programming.
Between 2005 and 2012, AIDS-related deaths fell by 30%
Of the 25 “All In” countries that represent 90% of deaths and
85% of new infections in adolescents, 18 (72%) are in sub-
Saharan Africa (8). “All In” aims for at least 90% of ALHIV to
among the global people living with HIV (PLHIV) population know their status, and part of the approach is to advocate for
(1); however mortality rose by 50% among adolescents liv- wider adolescent access to HIV testing at the country level
ing with HIV (ALHIV) (1,2). Globally, in 2013, an estimated using strategic information relevant to this population (8).
120,000 AIDS-related deaths occurred among adolescents Unfortunately, without concentrated efforts, sub-Saharan
aged 10–19 y, with 110,000 (nearly 92%) of these deaths occur- Africa may be left behind and may not meet this target by
ring in sub-Saharan Africa (3). This represents a significant 2020. This review highlights region-specific adolescent HIV
rise in global adolescent AIDS deaths from 71,000 in 2005 (4). studies and discusses challenges in, and opportunities for
AIDS is the number one killer of adolescents in Africa (5,6). providing wider access to timely HTC services for adoles-
To control the impact of AIDS on the lives of adolescents living cents in sub-Saharan Africa.

1
Clinical Department, Institute of Human Virology Nigeria, Abuja, Nigeria; 2Division of Epidemiology and Prevention, Institute of Human Virology, University of Maryland School of
Medicine, Baltimore, Maryland; 3Department of Pediatrics, University of Maryland School of Medicine, Baltimore, Maryland; 4Department of Paediatrics, University of Cape Coast,
Cape Coast, Ghana; 5Department of Child ­Dental Health and Institute of Public Health, Obafemi Awolowo University, Ile Ife, Nigeria; 6Department of Pediatrics, University of Nevada
Las Vegas, Las Vegas, Nevada; 7Department of Public Health, University of Nevada Las Vegas, Las Vegas, Nevada. Correspondence: Nadia Sam-Agudu (nsamagudu@ihvnigeria.org)
Received 17 April 2015; accepted 13 December 2015; advance online publication 16 March 2016. doi:10.1038/pr.2016.28

838  Pediatric Research       Volume 79 | Number 6 | June 2016 Copyright © 2016 International Pediatric Research Foundation, Inc.
HIV Testing for African Adolescents Review
UPTAKE OF ADOLESCENT HIV TESTING AND COUNSELING (in males/females) from Malawi (14). Similar to the adolescent
IN SUB-SAHARAN AFRICA group, WCA adults are experiencing the lowest HTC rates
In 2007, the WHO recommended provider-initiated testing while those in ESA countries are experiencing relatively higher
and counseling (PITC) as an opt-out approach to HTC, where rates. The WHO PITC, Adolescent Testing and Consolidated
healthcare workers provide testing as part of routine medical HIV Testing Service guidelines make testing recommen-
care or clinical management unless the client declines (10). This dations for all populations in low-level, concentrated and
was in contrast to the client-initiated voluntary counseling and generalized epidemics, but not specifically for mixed concen-
testing, where the client proactively seeks HIV testing on their trated-generalized epidemics (9,10,15). All populations are to
own. The goal of the PITC strategy is to increase opportuni- be offered PITC in generalized epidemics, and key population
ties for HIV testing and diagnosis, especially in high-burden adolescents are to be offered testing in all epidemic type set-
areas with low testing rates. With the PITC guidelines came a tings (9,10,15). Testing services with linkage to care are to be
recommendation to governments “to develop and implement made accessible for adolescents in concentrated and low-level
clear legal and policy frameworks” to address issues of con- epidemic settings (9,15). All three documents strongly recom-
sent and assent for minors including adolescents (10). Even for mend revision of age of consent policies to increase indepen-
client-initiated voluntary counseling and testing, issues of con- dent access to HTC for adolescents.
sent and assent remain for adolescent minors, and therefore
the presence of clear, well-communicated legal policies play a WILLINGNESS TO TEST AND BARRIERS TO HIV TESTING
critical role in HTC scale-up among adolescents. AND COUNSELING AMONG ADOLESCENTS IN SUB-
By 2010, 42 African countries, including all 18 All-In African SAHARAN AFRICA
countries, had adopted a PITC policy, however, the PITC poli- Studies show that the desire to be tested for HIV among ado-
cies were not universally applied across all populations in all lescents is relatively high. A WHO study combining data from
countries (11). The main population targeted was pregnant workshops among 98 adolescents in the Philippines, South
women, and by 2010, only 31 of the 42 countries offered PITC Africa and Zimbabwe with an online survey of 655 participants
to all adults, and PITC was offered to infants of HIV-positive from 92 countries indicated that approximately two-thirds
mothers, children on admission or in feeding centers in only of untested adolescents desired an HIV test (16). The WHO
10 countries (11). study included 13 of the 18 All In African countries. Individual
Table 1 shows rates of HIV testing among adolescents country studies and surveys also indicate strong desire to test:
who also received their results in the 18 All-In African coun- between 47.8 and 85.5% of adolescents and youth want to be
tries, using the most current available data between 2009 and tested for HIV in West/Central (17–20), East (18,21–23), and
2014. Among girls, the lowest rates were in Nigeria (4%), the southern Africa (24–26). The proportion of adolescents will-
Democratic Republic of Congo (DRC) (5%) and Côte d’Ivoire ing to test differed within and between some countries with
(10%), while the highest rates occurred in Uganda (31%), respect to factors including gender, geographical residence,
Lesotho (33%), and Malawi (44%). For boys, testing rates were socio-cultural norms, and HIV knowledge and risk perception
lowest in the DRC (1%), Nigeria (2%), and Côte d’Ivoire (5%) of participants. Overall, the proportion of adolescents willing
and highest in Swaziland (18%), Malawi (21%), and Rwanda to test was higher in later vs. earlier-conducted studies.
(24%) (8). These data reveal that the lowest HIV testing rates Given the low HTC rates, it appears that adolescents’ will-
among adolescents are occurring in West and Central African ingness to be tested is not matched by their HTC uptake,
(WCA) countries, while the highest rates are in East and and factors reducing access to testing need to be elicited and
southern African (ESA) countries. It is possible that the rela- addressed. The WHO adolescent HTC study evaluated barri-
tively lower rates of adolescent HTC in WCA countries stem ers to HTC, categorizing them into personal, social, cultural,
from the prevalence and/or type of epidemic in that region. or service-related (16). The most frequently expressed barrier
Adult HIV prevalence in WCA countries (median 1.6%) is to HTC among untested adolescents was fear, including fear
generally lower than in ESA countries (median 6.3%) (12). of needles, parents’ reaction to a positive result, AIDS-related
Furthermore, in contrast to ESA’s generalized epidemic, WCA illness, stigma/discrimination, and death (16). Interestingly,
presents more of a mixed (both generalized and concentrated) while ~20% of respondents expressed fear as a barrier, this pro-
epidemic within countries (13). This may make it more com- portion rose to ~53% among the African adolescents (16), sug-
plicated to locate and test HIV-infected individuals, and there- gesting that addressing multiple sources of fear (for example,
fore result in lower HTC coverage. Regardless, none of the debunking myths and exaggerations of truth with education
adolescent HTC rates in any African country approximate the and counseling) among African adolescents may be important
90% target that the All-In initiative aims for. While also falling to overcome barriers to testing. Other major barriers identi-
short of the 90% benchmark, reported adult (15–49 y) HTC fied in the WHO study were the impact of a positive ­diagnosis,
in the All-In countries have been higher than that of adoles- association of HTC with bad or high-risk behavior, lack of
cents. Drawing on data current between 2010 and 2013, adult information, perceived risk with respect to sexual exposure,
HTC rates were 12.6, 13.2, and 17.1% in Côte d’Ivoire, DRC, denial, poor attitudes of healthcare providers (poor confiden-
and Nigeria, respectively; higher values of 59.3% were reported tiality, insensitivity, and being judgmental), difficulty access-
from Uganda, 63.8% from Botswana and 51.2%/71.6% ing testing services (transportation, cost, long waiting times,

Copyright © 2016 International Pediatric Research Foundation, Inc. Volume 79 | Number 6 | June 2016      Pediatric Research  839
Review Sam-Agudu et al.

Table 1.  HIV statistics among adolescents in sub-Saharan Africaa,b


% Adolescents Estimated number % HIV prevalence
(15–19 y) of new infections among
HIV-tested and among adolescents adolescents
ALHIV Estimated Estimated
received resultsc (15–19 y), 2013 (15–19 y)c
Burden Rank, ALHIV Burden ALHIV Burden
2014 Country (10–19 y), 2014 (10–19 y), 2013 Female Male Female Male Female Male
1 South Africa 250,000 320,000 -d -d 45,000 8,800 5.6 0.7
2 Nigeria 200,000 160,000 4.0 2.0 12,000 5,300 - d
-d
3 Kenya 160,000 140,000 18.0 13.0 6,200 2,700 1.1 0.9
4 Mozambique 120,000 110,000 18.0 8.0 12,000 4,600 7.1 2.7
5 Tanzania 110,000 140,000 21.0 13.0 4,300 1,800 1.3 0.8
6 Zimbabwe 110,000 110,000 18.0 7.0 4,700 2,100 4.2 3.4
7 Uganda 100,000 110,000 31.0 17.0 10,000 4,500 3.0 1.7
8 Ethiopia 98,000 140,000 19.0 17.0 1,100 <500 0.2 0.0
9 Malawi 83,000 93,000 44.0 21.0 2,200 1,000 4.2 1.3
10 Zambia 65,000 79,000 22.0 10.0 3,100 1,900 5.7 3.6
11 Cameroon 39,000 41,000 15.0 7.0 2,700 1,200 2.0 0.4
12 Democratic Republic of the Congo 36,000 32,000 5.0 1.0 2,000 <1,000 0.7 0.2
13 Côte d’Ivoire 29,000 41,000 10.0 5.0 <1,000 <500 0.8 1.0
14 Rwanda 20,000 18,000 27.0 24.0 <500 <200 0.8 0.3
15 Botswana 17,000 11,000 -d -d <1,000 <500 5.0 2.4
16 Lesotho 15,000 21,000 33.0 12.0 2,000 <1,000 4.1 2.9
17 Swaziland 14,000 11,000 23.0 18.0 <1,000 <500 10.1 1.9
18 Namibia 11,000 13,000 29.0 14.0 <1,000 <500 -d -d
Among the highest ALHIV-burden sub-Saharan African countries targeted by All In to End Adolescent AIDS, in 2013, and where indicated, in 2014 (8). bData from UNICEF Global HIV
a

Database, October 2014 (3) and from All In to End Adolescent AIDS (8). cData compiled from most recent national surveys conducted between 2007 and 2014 (8). dNo available data (8).

service hours), and parent/guardian consent requirements 5 All In countries: Cameroon, Côte d’Ivoire, DRC, Nigeria,
(16). Other studies conducted across sub-Saharan Africa cor- and Tanzania (33) (Table 2). With the exception of Tanzania,
roborate with the WHO study with respect to barriers to ado- all of these countries are in West and Central Africa.
lescent HTC (18,20,22–24,26–32). These studies identified Lawmakers are often reluctant to reduce the minimum age
major barriers as fear of a positive test, especially among those of consent for sexual and reproductive health (SRH) ser-
sexually active, and fear of stigma and discrimination, includ- vices, including HTC, out of the desire to protect the child,
ing being ostracized by friends and family. Fear of loss of cur- who may be viewed as too young or immature (9,33). With
rent or future partners, and the potential psychological impact respect to HTC and SRH research among adolescents, these
of these consequences, including depression and suicide, were concerns have been countered with reassuring evidence and
also expressed by African adolescents (22–24,26,28,30,32). testing/recruitment approaches and strategies (34–37), how-
Due to its legal implications, and likely wide cross-regional ever, challenges still exist with enactment and implementa-
and country variation, age of consent for HTC amongst minors tion of laws supporting HTC for minors. Even where the
under age 18 y is treated separately. The next section singles law permits access to HTC by younger adolescents or where
out and discusses legal consent as relates to HTC among ado- parental/guardian consent can be sought, the behavior of
lescents in sub-Saharan Africa. healthcare providers may act as barriers due to the influence
of socio-cultural norms consistent with limiting dialogue
LEGAL AGE OF CONSENT AND ADOLESCENT HIV TESTING about sex, restricting services for HTC, judgmental attitudes
IN SUB-SAHARAN AFRICA during service provision to adolescents and determining
One of the major barriers to the uptake of HTC among ado- appropriateness of caregivers to give consent (16,33,37–41).
lescents in sub-Saharan Africa is the requirement of paren- Furthermore, confusion about testing guidelines and regu-
tal/guardian consent for minors (33). The WHO reports lations and concern for the ward’s increased vulnerability
that of 40 countries in the African region with defined laws if HIV-positive, may limit healthcare providers’ offering of
on age of consent for HTC, less than half (19, 47.5%) have HTC as PITC (41). Nevertheless, the involvement of fam-
enacted laws supporting independent HTC to adolescents ily in an ALHIV’s decision to test and their ward’s ability
less than 18 y of age (33). The remaining 21 countries that to cope after disclosure of a positive test has been shown to
do not have legislation supporting HTC for minors include be critical (28). As much as independent adolescent testing

840  Pediatric Research       Volume 79 | Number 6 | June 2016 Copyright © 2016 International Pediatric Research Foundation, Inc.
HIV Testing for African Adolescents Review
Table 2.  Age of consent for sexual activity, marriage and for HIV testing and counseling, sub-Saharan African countriesa
Legal age of Legal age of Legal age of consent, years, for
Estimated consent for consent for marriage (early marriage age for % Young women Adolescent pregnancy
ALHIV Burden independent consensual girls, supported under customary (20–24 y) married or rate (per 1,000 females
Country (10–19 y), 2014 HTCb sexb,c and/or religious practicec in union by age 18 yd aged 10–19 y)d
South Africa 250,000 12 y 12 y 18 (12) 6.0 54
Nigeria 200,000 18 y 18 y 18 (at puberty) 43.0 122
Kenya 160,000 No age limite 18 y 16 (at puberty) 26.0 106
Mozambique 120,000 16 y 18 y 21 (under 15) 48.0 166
Tanzania 110,000 18 y 18 y 18 (12) 37.0 128
Zimbabwe 110,000 16 y 16 y 18 (no minimum) 31.0 112
Uganda 100,000 12 y 18 y 18 (12) 40.0 146
Ethiopia 98,000 15 y 18 y 18 (7) 41.0 87
Malawi 83,000 13 y 16 y 18 (12) 50.0 157
Zambia 65,000 16 y 16 y 16 (no minimum) 42.0 151
Cameroon 39,000 18 y 18 y 18 (9) 38.0 128
Democratic 36,000 18 y 14 y girls/18 y 18 (_f ) 39.0 135
Republic of boys
the Congo
Côte d’Ivoire 29,000 18 y 18 y 18 girls, 20 boys (14) 33.0 125
Rwanda 20,000 15 y 18 y 21 (-f ) 8.0 41
Botswana 17,000 No age limit e
16 y 18 (- )f
-f
51
Lesotho 15,000 12 y 18 y 16 girls,18 boys (no minimum) 19.0 92
Swaziland 14,000 16 y 16 y 18 (13) 7.0 89
Namibia 11,000 16 y 16 y 18 (-f ) 9.0 74
a
Among the highest ALHIV-burden sub-Saharan African countries targeted by All In to End Adolescent AIDS (8). bData from WHO: Adolescent consent to HIV testing: a review of current
policies and issues in sub-Saharan Africa (33). cData from Country Reports on Human Rights Practices (Forced and Early Marriage, and Sexual Exploitation of Children), 2013 (43).
Only data on legal age not requiring parental approval are displayed. dMost recent data up until 2013. Data from UNICEF, State of the World’s Children Report, 2014 (42). eAll or most
adolescents are eligible under several considerations including showing maturity, of reproductive age, married, pregnant, or engaged in high-risk behavior. fNo available data.

should be made available, a supportive and involved family and comprehensive approach to adolescent sexual health,
is desirable for optimal outcomes. including family planning and HTC. With the exception
of Rwanda, all the All-In African countries are also priority
TESTING PREGNANT AND NONPREGNANT FEMALE countries for the elimination of mother-to-child transmis-
ADOLESCENTS IN SUB-SAHARAN AFRICA sion of HIV (45). Pregnant adolescent females living with HIV
In many African countries where adolescents have limita- are a subgroup of African ALHIV that has received relatively
tions in access to HTC and HIV care, early marriage at <15 little attention. These adolescents often have to contend with
y, especially amongst girls, is culturally and/or legally permis- the double stigma of teen or preteen pregnancy and HIV; in
sible (Table 2) (33,42,43). These marriages are often arranged African societies, both of these phenomena are regarded as
by parents and guardians without input from the adolescent indicative of sexual promiscuity. Unless pre- and early preg-
(33,42). Among married adolescent girls age 15–19 y in six nancy HTC services for this marginalized group are scaled up,
West African countries, only 16–26% state that they have a exposed infants and uninfected partners will continue to be at
final say in their own healthcare (44). In this regard, early mar- risk for HIV infection.
riage and parenthood where not consistent with empowerment To date, only two studies, both from South Africa, have spe-
to make choices such as self-testing for HIV, is not necessarily cifically evaluated HTC among pregnant adolescents accessing
a step toward adulthood and independence. The concept of prevention of mother-to-child transmission of HIV (PMTCT)
“emancipated minor” in many of these countries is either non- services (46,47). One study was a cross-sectional survey in
existent or poorly defined (33,43), making access to testing and Kwazulu Natal (KZN) (46); the other was a cohort study with
other HIV/SRH-related services difficult for most adolescents. follow-up, in Eastern Cape (47). Ever-tested for HIV rates were
In addition to relatively high HIV incidence, sub-Saharan similar (≥ 98%) between adolescent and adult mothers in the
African countries have some of the highest pregnancy rates KZN study (46), likely facilitated by legislation supporting
among adolescents in the world (Table 1). The high rate of ado- HTC for adolescents 12 y and older in South Africa (33). In
lescent pregnancies reflects poor access to family planning for the Eastern Cape study, adolescents were 1.4 times less likely to
this population and indicates the need for a more integrated have tested for HIV prior to booking (47). Compared to adult

Copyright © 2016 International Pediatric Research Foundation, Inc. Volume 79 | Number 6 | June 2016      Pediatric Research  841
Review Sam-Agudu et al.

women, adolescents experienced later entry into care, lower initiatives targeted to pediatric and adolescent HIV treatment
ART uptake or inappropriate ART administration, lower early and prevention in sub-Saharan Africa such as the Accelerating
infant diagnosis rates, and increased mother-to-child trans- Children’s HIV/AIDS Treatment and DREAMS initiatives
mission of HIV (MTCT), stillbirth, and mortality (46,47). (55–57) have involved few or none of the high-burden West
These studies highlight gaps in PMTCT service delivery for and Central African countries. There have been high-level
adolescents and higher risk of MTCT among adolescent HIV- calls for quality strategic information and increased HIV/
positive mothers, even in the setting of optimized legal access SRH research participation among all adolescents, especially
to HTC. It is evident that legal access to HTC should be cou- in Africa (5,6,9). Southern and East Africa have led the region
pled with timeliness of testing and successful linkage to com- in implementing innovative approaches to adolescent HIV
prehensive services, particularly among adolescent females services, leaving West and Central Africa trailing behind (54).
before and during pregnancy. However, sub-Saharan Africa as a whole needs more efforts
to improve HIV diagnosis and access to quality care and to
THE CASE FOR EXPANDING ADOLESCENT ACCESS TO reduce AIDS-related deaths among adolescents (8,9,33). One
HIV TESTING AND COUNSELING BY LOWERING AGE OF of the first steps in changing the status quo is the identifica-
CONSENT tion of as many ALHIV as possible: the road to 90-90-90 for
In 2014, the Joint United Nations Programme on HIV/AIDS African adolescents starts with wider access to independent
(UNAIDS) introduced new global HIV targets to be achieved HTC.
by 2020. These targets were dubbed “90-90-90”: to have 90%
of all people living with HIV knowing their status, 90% of all ENABLING STRATEGIES AND INTERVENTIONS TO IMPROVE
people diagnosed with HIV receiving sustained antiretroviral ADOLESCENT HIV TESTING AND COUNSELING
therapy, and 90% of all people receiving antiretroviral therapy A rights-based approach should guide access to adolescent SRH
achieving viral suppression (48). Up to 81% of African adoles- and HIV care (37,58), including testing for HIV. Adolescents
cents already living with HIV do not know their HIV status should be informed of their right to access stigma-free HIV
(38,39,49–51). One study from Zimbabwe reported that 80% testing and related services provided by respectful, compe-
of ALHIV in their study cohort were infected from MTCT and tent staff, and they should participate in the development and
15% from sexual transmission (51). Apart from the large gap implementation of relevant policies and practices. In order to
in access to HTC, the lack of adolescents’ knowledge of their achieve this, an enabling environment should be created within
HIV status is partially attributable to low disclosure rates of legal, socio-cultural, research and healthcare delivery contexts.
HIV-positive status previously known to others (39,50,52). Additionally, interventions should target barriers within these
Expanding independent access to HTC allows maturing ado- different contexts while taking transmission dynamics into
lescents, especially the perinatally-infected and those not dis- consideration. For example, adolescents under age 14 y have
closed to, to discover their HIV status and to begin to take no significant gender differences with respect to HIV preva-
charge of their own health (25,40). lence, suggesting a nonsexual mode of HIV acquisition (59).
Restriction of independent HTC as an SRH service to indi- However, beyond 14 y, female adolescents have much higher
viduals 18 y and older can be argued to be slowing progress HIV incidence and prevalence as compared to males (7,8,59–61)
in the provision of appropriate, impactful interventions for (Table 1). Pregnant adolescent females (46,47), adolescents
HIV prevention and quality HIV care amongst African ado- with early sexual debut, married, or partnered but living sepa-
lescents (33,53). With the exception of Tanzania, ESA All In rately, engaging in transactional sex, especially in rural areas
countries have more adolescent-friendly HTC laws and have (62,63), having multiple or older sexual partners (59,60,64),
higher adolescent HTC coverage than WCA countries, whose and those experiencing high mobility and labor migration
laws restrict self-consent for HTC to 18 y and above (Tables (65,66), have also been identified to be at increased risk of
1and 2). Legally-enabling environments are likely to promote HIV infection and unfavorable outcomes. Lastly, the signifi-
not only the provision of clinical services but the conduct of cant proportions of perinatally-infected individuals surviving
research and the establishment of targeted health programs into young adolescence and young adulthood should not be
relevant to HIV among adolescents. Subsequently, adolescent- overlooked (51,61,67). While advocating for and strengthen-
specific research findings can contribute to impactful policies ing HTC uptake and coverage, linkage to quality care should
on HIV prevention and control among African adolescents. be available to make HTC ultimately beneficial. Recent studies
Therefore, restrictions on independent access to critical adoles- have cited early loss-to-follow-up, refusal of care, and nonre-
cent SRH services including HTC may be contributing to a lack ceipt of baseline CD4 as barriers to engagement in care among
of, or weak policies for this population. This may be especially newly-identified ALHIV (68–70). We recommend the fol-
true for WCA, where the HIV epidemic is of a mixed nature lowing measures to create an enabling environment for HTC
(13) and PLHIV, including adolescents, may be more difficult to among adolescents, including those at highest risk:
reach, test, and treat with current strategies and policies.
Recent cross-continental and global technical reports • Enactment of laws expressly permitting independent
and guidelines have featured little or no input from the access to HTC for adolescents less than 18 y of age
WCA region (9,54). Furthermore, recent significant funding across the WHO Africa region, but especially in WCA.

842  Pediatric Research       Volume 79 | Number 6 | June 2016 Copyright © 2016 International Pediatric Research Foundation, Inc.
HIV Testing for African Adolescents Review
The median age at sexual debut or age at which custom- • Provision of adolescent-friendly healthcare facility HTC
ary/traditional marriages are allowed can be used as a points of service, with strategies in place to tightly link
benchmark. It is critical for every country to have age of and retain newly-diagnosed adolescents in care.
consent legislation that takes age of first exposure to sex- • Expanding testing opportunities beyond healthcare
ual activity (within and outside of marriage) into con- facilities, specifically for female adolescents, for example
sideration. This is especially important for girls. These among rural or out-of-school youth, street hawkers and
laws should also be consistent with what HTC and SRH market traders, in boarding schools, at points of pur-
guidelines recommend in each country. Consultations chase for condoms, and in antenatal care clinics. Given
among stakeholders, including adolescents and lawmak- the high birth rates and worse maternal-infant outcomes
ers, should be held to determine timeline and reference for HIV- infected adolescent mothers, expanded HTC
ages for revising HTC legislation. WCA countries can among adolescent females should be coupled with treat-
leverage on lessons learned from ESA countries that ment for Sexually-Transmitted Infections and family
have already lowered their age of consent for HTC, to planning to prevent unwanted pregnancies.
move this agenda forward. • Strategies to improve caregiver involvement in test-
• Development of guidelines and laws for adolescents to ing, post-test disclosure and access to care for ALHIV
independently provide consent for participation in SRH regardless of mode of access to testing. Healthcare work-
and HIV research. These guidelines and laws should be ers should counsel and support parents and guardians to
consistent with those governing the age of consent for disclose to their adolescent wards. In addition, parents
routine SRH and HIV services. WCA countries have an and guardians of independently-tested ALHIV who need
opportunity to legislate concurrently for HIV/SRH ser- or wish to disclose should be educated and counseled to
vices and related research since few countries may have accept the positive diagnosis and to support their wards.
pre-existing laws to that effect. • Behavior change communications programs, ideally
• Involve both uninfected adolescents and ALHIV in with post-implementation measurement of impact,
policy-making and practice, from grassroots dialogue targeted specifically to adolescent, family, healthcare
as advocates and advisors, to participation in health- worker, law- and policy-maker stakeholders.
care delivery as peer counselors. Specifically for WCA, • Engaging ALHIV and families of adolescents living
adolescents can play a role in increasing identification positively with HIV to provide education and improve
of undiagnosed ALHIV in highly-affected communities, uptake of HTC among their untested peers, within and
groups or social circles. Other PLHIV who have already outside of the healthcare facility. Reassurance and alle-
been tested and in care, including family members, can viation of commonly-held testing fears among adoles-
serve as index clients whose adolescent contacts may be cents by experienced healthcare workers, other PLHIV
tested for increased coverage. and educated family members may make a large impact
• Specialized certificate- or license-granting training on on poor HTC uptake.
adolescent HIV, adolescent SRH service provision and
adolescent health-related legislature, for healthcare pro-
viders. Emphasis should be put on skill-building in ado- CONCLUSION
lescent drug adherence and SRH counseling. In sub-Saharan Africa, where adolescent HIV burden is high,
• HIV seroprevalence, SRH surveys, and other HIV-related testing rates are low and outcomes most grim, several barriers
data should include younger adolescents 10–14 y old as continue to limit access to HTC. Adolescents desire to be tested
well as disaggregate data to reflect trends in 10- to 19-y for HIV, but those infected are often identified late or not at
olds. Health surveys and other epidemiologic HIV data all, due to late or restricted access often influenced by cultural
often exclude younger adolescents and have poorly- norms and biases. Removing legal barriers is only one step
defined or poorly-disaggregated age categories with toward adolescents knowing their HIV status and accessing
respect to adolescents (54,67). This limits the ability of early and quality HIV care. Robust implementation research
funders and policy-makers to make evidence-based rec- studies are needed to provide new knowledge to improve pro-
ommendations positively impacting on all adolescents gramming and policy for highly accessible HIV testing and
and has further implication for mixed epidemic countries care, such as: improved PMTCT service access for pregnant
where detailed subnational data is necessary to know HIV-positive adolescents, community-based interventions to
where testing should be concentrated. Furthermore, increase adolescent HTC in rural hard-to-reach communities,
more data is needed on the source of infection for ALHIV school-based interventions that integrate HIV education and
(behavioral, perinatal through MTCT, or other) (7), espe- on-site HIV testing, family involvement, and mobile testing.
cially in WCA, for targeted test and treat strategies. This paper adds its voice to the calls for high-burden African
countries to urgently address HIV testing and counseling bar-
Specific programming and research interventions to improve riers towards the improvement of HIV treatment outcomes for
HTC among African adolescents should include the following: all infected adolescents.

Copyright © 2016 International Pediatric Research Foundation, Inc. Volume 79 | Number 6 | June 2016      Pediatric Research  843
Review Sam-Agudu et al.
ACKNOWLEDGMENTS 19. Federal Ministry of Health Nigeria. National HIV & AIDS and Reproduc-
We thank the African adolescents with whom we have worked over the tive Health Survey (NARHS Plus II) 2013. http://nascp.gov.ng/demo/wp-
years for their perseverance as we elucidate best practices for keeping them content/uploads/2014/02/NARHS-Plus-2012-Final-18112013.pdf.
in excellent health. Above all, we thank them for educating us as we work 20. Haddison  EC, Nguefack-Tsagué  G, Noubom  M, Mbatcham  W,

towards this goal. Ndumbe PM, Mbopi-Kéou FX. Voluntary counseling and testing for HIV
among high school students in the Tiko health district, Cameroon. Pan Afr
STATEMENT OF FINANCIAL SUPPORT Med J 2012;13:18.
There was no financial support for this work. 21. Mbonye AK, Wamono F. Access to contraception and HIV testing among
Disclosure: The authors have no conflicts of interest to disclose. young women in a peri-urban district of Uganda. Int J Adolesc Med Health
2012;24:301–6.
References 22. Mwangi RW, Ngure P, Thiga M, Ngure J. Factors influencing the utilization
1. UNAIDS. Global Report: UNAIDS Report on the Global AIDS Epidemic of Voluntary Counselling and Testing services among university students
2013. http://www.unaids.org/en/media/unaids/contentassets/documents/ in Kenya. Glob J Health Sci 2014;6:84–93.
epidemiology/2013/gr2013/UNAIDS_Global_Report_2013_en.pdf. 23. Sisay S, Erku W, Medhin G, Woldeyohannes D. Perception of high school
2. Kasedde  S, Luo  C, McClure  C, Chandan  U. Reducing HIV and AIDS students on risk for acquiring HIV and utilization of voluntary counsel-
in adolescents: opportunities and challenges. Curr HIV/AIDS Rep ing and testing (VCT) service for HIV in Debre-berhan Town, Ethiopia: a
2013;10:159–68. quantitative cross-sectional study. BMC Res Notes 2014;7:518.
3. UNICEF. Global HIV Database, 2014. http://data.unicef.org/hiv-aids/ 24. MacPhail CL, Pettifor A, Coates T, Rees H. “You must do the test to know
global-trends. your status”: attitudes to HIV voluntary counseling and testing for ado-
4. UNICEF. Towards an AIDS-Free Generation: Children and AIDS-Sixth lescents among South African youth and parents. Health Educ Behav
Stocktaking Report, 2013. http://www.childrenandaids.org/files/str6_full_ 2008;35:87–104.
report_29-11–2013.pdf. 25. Ferrand  RA, Trigg  C, Bandason  T, et al. Perception of risk of vertically
5. World Health Organization. Health for the World’s Adolescents: a Sec- acquired HIV infection and acceptability of provider-initiated testing
ond Chance in the Second Decade, 2014. http://apps.who.int/iris/bit- and counseling among adolescents in Zimbabwe. Am J Public Health
stream/10665/112750/1/WHO_FWC_MCA_14.05_eng.pdf?ua=1. 2011;101:2325–32.
6. UNICEF. 2014 Statistical Update: Children, Adolescents and AIDS, 2014. 26. Fako  TT. Social and psychological factors associated with willingness
www.childrenandaids.org/files/Stats_Update_11-27.pdf. to test for HIV infection among young people in Botswana. AIDS Care
7. Idele P, Gillespie A, Porth T, et al. Epidemiology of HIV and AIDS among 2006;18:201–7.
adolescents: current status, inequities, and data gaps. J Acquir Immune 27. Denison  JA, McCauley  AP, Dunnett-Dagg  WA, Lungu  N, Sweat  MD.
Defic Syndr 2014;66 Suppl 2:S144–53. HIV testing among adolescents in Ndola, Zambia: how individual, rela-
8. UNAIDS, UNICEF. All in to End Adolescent AIDS, 2015. http://allintoen- tional, and environmental factors relate to demand. AIDS Educ Prev
dadolescentaids.org/. 2009;21:314–24.
9. World Health Organization. HIV and Adolescents: Guidance for HIV 28. Denison JA, McCauley AP, Dunnett-Dagg WA, Lungu N, Sweat MD. The
Testing and Counselling and Care for Adolescents Living with HIV, 2013. HIV testing experiences of adolescents in Ndola, Zambia: do families and
http://www.who.int/iris/bitstream/10665/94334/1/9789241506168_eng. friends matter? AIDS Care 2008;20:101–5.
pdf?ua=1. 29. Godia PM, Olenja JM, Hofman JJ, van den Broek N. Young people’s per-
10. WHO. Guidance on Provider-initiated HIV Testing and Counsel-
ception of sexual and reproductive health services in Kenya. BMC Health
ing in Health Facilities, 2007. http://whqlibdoc.who.int/publica- Serv Res 2014;14:172.
tions/2007/9789241595568_eng.pdf. 30. Yahaya LA, Jimoh AA, Balogun OR. Factors hindering acceptance of HIV/
11. Baggaley R, Hensen B, Ajose O, et al. From caution to urgency: the evolu- AIDS voluntary counseling and testing (VCT) among youth in Kwara
tion of HIV testing and counselling in Africa. Bull World Health Organ State, Nigeria. Afr J Reprod Health 2010;14:159–64.
2012;90:652–658B. 31. Uzochukwu B, Uguru N, Ezeoke U, Onwujekwe O, Sibeudu T. Voluntary
12. UNAIDS. UNAIDS Report on the Global AIDS Epidemic, 2015. http:// counseling and testing (VCT) for HIV/AIDS: a study of the knowledge,
www.unaids.org/en/resources/documents/2015/HIV_estimates_with_ awareness and willingness to pay for VCT among students in tertiary insti-
uncertainty_bounds_1990-2014. tutions in Enugu State Nigeria. Health Policy 2011;99:277–84.
13. World Bank Global HIV/AIDS Program. West Africa HIV/AIDS
32. Munthali  AC, Mvula  PM, Maluwa-Banda  D. Knowledge, attitudes and
Epidemiology and Response Synthesis. Characterisation of the practices about HIV testing and counselling among adolescent girls in
HIV Epidemic and Response in West Africa: Implications for Pre- some selected secondary schools in Malawi. Afr J Reprod Health 2013;17
vention, 2008. http://siteresources.worldbank.org/INTHIVAIDS/ (4 Spec No):60–8.
Resources/375798-1132695455908/WestAfricaSynthesisNov26.pdf. 33. World Health Organization. Adolescent Consent to HIV Testing: a Review
14. UNAIDS. 2014 Progress Reports Submitted by Countries, 2014. http:// of Current Policies and Issues in Sub-Saharan Africa, 2013. http://www.
www.unaids.org/en/dataanalysis/knowyourresponse/countryprogressrep ncbi.nlm.nih.gov/books/NBK217954/#annex15.s1.
orts/2014countries/. 34. Stanford  PD, Monte  DA, Briggs  FM, et al.; Reaching for Excellence in
15. World Health Organization. Consolidated Guidelines on HIV Test-
Adolescent Care and Health Project. Recruitment and retention of ado-
ing Services. 5Cs: Consent, Confidentiality, Counselling, Cor- lescent participants in HIV research: findings from the REACH (Reaching
rect Results and Connection, 2015. http://apps.who.int/iris/bitstr for Excellence in Adolescent Care and Health) Project. J Adolesc Health
eam/10665/179870/1/9789241508926_eng.pdf?ua=1. 2003;32:192–203.
16. World Health Organization. The Voices, Values and Preference of Ado- 35. Gilbert  AL, Knopf  AS, Fortenberry  JD, Hosek  SG, Kapogiannis  BG,

lescents on HIV Testing and Counselling, 2013. http://www.who.int/iris/ Zimet GD. Adolescent Self-Consent for Biomedical Human Immunode-
bitstream/10665/95143/1/WHO_HIV_2013.135_eng.pdf. ficiency Virus Prevention Research. J Adolesc Health 2015;57:113–9.
17. Babalola  S. Readiness for HIV testing among young people in north- 36. Bekker LG, Slack C, Lee S, Shah S, Kapogiannis B. Ethical issues in adoles-
ern Nigeria: the roles of social norm and perceived stigma. AIDS Behav cent HIV research in resource-limited countries. J Acquir Immune Defic
2007;11:759–69. Syndr 2014;65 Suppl 1:S24–8.
18. Biddlecom AE, Munthali A, Singh S, Woog V. Adolescents’ views of and 37. Mburu G, Hodgson I, Teltschik A, et al. Rights-based services for adoles-
preferences for sexual and reproductive health services in Burkina Faso, cents living with HIV: adolescent self-efficacy and implications for health
Ghana, Malawi and Uganda. Afr J Reprod Health 2007;11:99–110. systems in Zambia. Reprod Health Matters 2013;21:176–85.

844  Pediatric Research       Volume 79 | Number 6 | June 2016 Copyright © 2016 International Pediatric Research Foundation, Inc.
HIV Testing for African Adolescents Review
38. Mburu G, Hodgson I, Kalibala S, et al. Adolescent HIV disclosure in Zam- 55. The United States President’s Emergency Plan for AIDS Relief. DREAMS:
bia: barriers, facilitators and outcomes. J Int AIDS Soc 2014;17:18866. Working Together for an AIDS-Free Future for Girls, 2014. http://www.
39. Kidia KK, Mupambireyi Z, Cluver L, Ndhlovu CE, Borok M, Ferrand RA. pepfar.gov/partnerships/ppp/dreams/index.htm.
HIV status disclosure to perinatally-infected adolescents in Zimbabwe: a 56. Birx  D. PEPFAR, Nike Foundation and Gates Foundation Partnership
qualitative study of adolescent and healthcare worker perspectives. PLoS Restores Hope for an AIDS-free Future for Girls, 2014. https://blogs.state.
One 2014;9:e87322. gov/stories/2014/12/09/pepfar-nike-foundation-and-gates-foundation-
40. Ramirez-Avila L, Nixon K, Noubary F, et al. Routine HIV testing in adoles- partnership-restores-hope-aids-free.
cents and young adults presenting to an outpatient clinic in Durban, South 57. US President’s Emergency Plan for AIDS Relief. Accelerating Children’s
Africa. PLoS One 2012;7:e45507. HIV/AIDS Treatment Initiative, 2014. http://www.pepfar.gov/documents/
41. Kranzer K, Meghji J, Bandason T, et al. Barriers to provider-initiated test- organization/232012.pdf.
ing and counselling for children in a high HIV prevalence setting: a mixed 58. Folayan  MO, Harrison  A, Odetoyinbo  M, Brown  B. Tackling the sexual
methods study. PLoS Med 2014;11:e1001649. and reproductive health and rights of adolescents living with HIV/AIDS:
42. UNICEF. State of the World’s Children Report: 2014 Statistical Tables, a priority need in Nigeria. Afr J Reprod Health 2014;18(3 Spec No):
2014. http://www.unicef.org/sowc2014/numbers/documents/english/ 102–8.
SOWC2014_In%20Numbers_28%20Jan.pdf. 59. Gregson S, Nyamukapa CA, Garnett GP, et al. Sexual mixing patterns and
43. United States Department of State. Country Reports on Human Rights Prac- sex-differentials in teenage exposure to HIV infection in rural Zimbabwe.
tices, Africa, 2013. http://www.state.gov/j/drl/rls/hrrpt/2013/af/index.htm. Lancet 2002;359:1896–903.
44. UNAIDS. The Gap Report 2014: Adolescent Girls and Young Women, 60. Kembo J. Risk factors associated with HIV infection among young persons
2014. http://www.unaids.org/node/43455. aged 15-24 years: evidence from an in-depth analysis of the 2005-06 Zim-
45. The Interagency Task Team for the Prevention of HIV in Pregnant Women babwe Demographic and Health Survey. SAHARA J 2012;9:54–63.
Mothers and Children. Priority Countries, 2015. http://www.emtct-iatt. 61. Mahy M, Garcia-Calleja JM, Marsh KA. Trends in HIV prevalence among
org/priority-countries/. young people in generalised epidemics: implications for monitoring the
46. Horwood C, Butler LM, Haskins L, Phakathi S, Rollins N. HIV-infected HIV epidemic. Sex Transm Infect 2012;88 Suppl 2:i65–75.
adolescent mothers and their infants: low coverage of HIV services and 62. Aboki H, Folayan MO, Daniel’and U, Ogunlayi M. Changes in sexual risk
high risk of HIV transmission in KwaZulu-Natal, South Africa. PLoS One behavior among adolescents: is the HIV prevention programme in Nigeria
2013;8:e74568. yielding results? Afr J Reprod Health 2014;18(3 Spec No):109–17.
47. Fatti G, Shaikh N, Eley B, Jackson D, Grimwood A. Adolescent and young 63. Folayan MO, Adebajo S, Adeyemi A, Ogungbemi KM. Differences in sex-
pregnant women at increased risk of mother-to-child transmission of HIV ual practices, sexual behavior and HIV risk profile between adolescents and
and poorer maternal and infant health outcomes: A cohort study at public young persons in rural and urban Nigeria. PLoS One 2015;10:e0129106.
facilities in the Nelson Mandela Bay Metropolitan district, Eastern Cape, 64. Edelstein ZR, Santelli JS, Helleringer S, et al. Factors associated with inci-
South Africa. S Afr Med J 2014;104:874–80. dent HIV infection versus prevalent infection among youth in Rakai,
48. UNAIDS. 90-90-90: An Ambitious Treatment Target to Help End the AIDS Uganda. J Epidemiol Glob Health 2015;5:85–91.
Epidemic, 2014. http://www.unaids.org/sites/default/files/media_asset/90- 65. Schuyler AC, Edelstein ZR, Mathur S, et al. Mobility among youth in Rakai,
90-90_en_0.pdf. Uganda: Trends, characteristics, and associations with behavioural risk
49. Vreeman  RC, Gramelspacher  AM, Gisore  PO, Scanlon  ML, Nyan-
factors for HIV. Glob Public Health 2015:1–18.
diko  WM. Disclosure of HIV status to children in resource-limited set- 66. Harrison  A, Colvin  CJ, Kuo  C, Swartz  A, Lurie  M. Sustained high HIV
tings: a systematic review. J Int AIDS Soc 2013;16:18466. incidence in young women in Southern Africa: social, behavioral, and
50. Arrivé E, Dicko F, Amghar H, et al.; Pediatric IeDEA West Africa Work- structural factors and emerging intervention approaches. Curr HIV/AIDS
ing Group. HIV status disclosure and retention in care in HIV-infected Rep 2015;12:207–15.
adolescents on antiretroviral therapy (ART) in West Africa. PLoS One 67. Lowenthal ED, Bakeera-Kitaka S, Marukutira T, Chapman J, Goldrath K,
2012;7:e33690. Ferrand  RA. Perinatally acquired HIV infection in adolescents from
51. Ferrand  RA, Munaiwa  L, Matsekete  J, et al. Undiagnosed HIV infection sub-Saharan Africa: a review of emerging challenges. Lancet Infect Dis
among adolescents seeking primary health care in Zimbabwe. Clin Infect 2014;14:627–39.
Dis 2010;51:844–51. 68. Tanner AE, Philbin MM, Duval A, Ellen J, Kapogiannis B, Fortenberry JD;
52. Mutumba M, Musiime V, Tsai AC, et al. Disclosure of HIV status to perina- Adolescent Trials Network for HIV/AIDS Interventions. “Youth friendly”
tally infected adolescents in urban Uganda: a qualitative study on timing, clinics: considerations for linking and engaging HIV-infected adolescents
process, and outcomes. J Assoc Nurses AIDS Care 2015;26:472–84. into care. AIDS Care 2014;26:199–205.
53. Folayan  MO, Haire  B, Harrison  A, Odetoyingbo  M, Fatusi  O, Brown  B. 69. Katz IT, Essien T, Marinda ET, et al. Antiretroviral therapy refusal among
Ethical issues in adolescents’ sexual and reproductive health research in newly diagnosed HIV-infected adults. AIDS 2011;25:2177–81.
Nigeria. Dev World Bioeth 2014;15:191–8. 70. Nkala B, Khunwane M, Dietrich J, et al. Kganya Motsha Adolescent Centre:
54. Pitorak H, Bergmann H, Fullem A, Duffy M. Mapping HIV Services and Pol- a model for adolescent friendly HIV management and reproductive health
icies for Adolescents: A Survey of 10 Countries in Sub-Saharan Africa. 2013. for adolescents in Soweto, South Africa. AIDS Care 2015;27:697–702.

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