Articles

Diagnosis and case finding according to key partner

risk populations of people living with HIV in Nigeria: A
retrospective analysis of community-led index partner
testing services
Amobi Onovo,a,c* Abiye Kalaiwo,a Angela Agweye,a Godwin Emmanuel,b and Olivia Keiserc
a
Office of HIV/AIDS and TB, US Agency for International Development, Nigeria
b
Heartland Alliance Nigeria LTD, Nigeria
c
Institute of Global Health, University of Geneva, Switzerland

Summary
Background The HIV epidemic in Nigeria is concentrated in Key Populations (KP), people who inject drugs EClinicalMedicine
(PWID), men who have sex with men (MSM), female sex workers (FSW), and partners of people living with HIV. 2022;43: 101265
Published online xxx
Due to stigma and discrimination, these groups have low access to HIV testing services (HTS) and linkage to treat-
https://doi.org/10.1016/j.
ment is challenging. To address this gap, index partner testing, targeting sexual contacts and injecting partners of eclinm.2021.101265
KP index clients, was introduced in 2017.

Methods The study was a retrospective analysis of community-led HIV index partner testing-involving review of sec-
ondary data from partner notification services registers. Between October 1, 2018, and September 30, 2019, HIV test-
ing as part of index partner testing services was offered at nightclubs, hotels, and community-based ART clinics in
the states of Akwa Ibom, Cross River, and Lagos. Index testing was assisted by peer navigators. We used provider
and passive Partner Notification (PN) methods. In-person and social network methods were used to recruit partners
of KP. We described the implementation of index partner testing services as part of the national KP program, ana-
lyzed PN delivery models, and calculated HIV seropositivity among persons who underwent Index Partner Testing.
One-Way ANOVA and Tukey-HSD test were performed to determine whether the differences in mean HIV seropos-
itivity between partners are statistically significant.

Findings PN was predominantly done through provider referral 5,159 (68.3%) and passive/client referral 2,278
(30.1%). A total of 3,119 index partners; 1,322 FSW (42.4%), 1,255 MSM (40.2%) and 542 PWID (17.4%) identified
8,989 sexual and injecting partners (index partner ratio 1:2.9). Among the partners, 7,556 (84.1%) were first-time
testers, and 79.4% (5,999) of male partners tested. Of the 3,753 (49.7%) partners who tested HIV-positive, 3,492
(93.0%) were enrolled in HIV care. HIV seropositivity rate was 65.5% (1,021/1,557) among females and 45.5%
(2,732/5,999) among males and was disproportionately higher among PWID injecting partners 99.1% (581/586),
PWID sexual partners 98.9% (433/438) and MSM sexual partners 95.6% (605/633) in Cross river compared with
71.4% (575/805) in FSW sexual partners.

Interpretations Including index partner testing as part of a community-led HTS can help improve HIV case-finding
approach for KP, particularly for reaching first-time testers, male KP, and persons not yet diagnosed with HIV. Scale-
up of index partner testing within community-led HTS is essential for achieving the United Nations 95−95−95
goals.

Funding This research received no specific grant from any funding agency in the public, commercial or not-for-
profit sectors.

Copyright Ó 2021 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/by/4.0/)

*Corresponding author at: Institute of Global Health, Univer- Introduction

sity of Geneva, Switzerland. People’s knowledge of their own, and their partner’s,
E-mail address: [email protected] human immunodeficiency virus (HIV) status is essen-
(A. Onovo). Amobi Onovo, A retrospective analysis of commu- tial to the success of the global HIV response. The over-
nity-led index partner testing services, https://doi.org/10.1016/ arching goals of providing HIV testing services (HTS)
j.eclinm.2021.101265.

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inhibit the ability of the HIV or other types of retrovi-

Research in context ruses to multiply in the body. The growing availability
and use of rapid diagnostic tests have made it possible
Evidence before this study to increase task sharing. This has enabled HTS to also
Recent systematic reviews show that KP's low uptake of be delivered by trained lay providers and to be imple-
HTS is often due to hostile services, fear of stigma, dis- mented in more targeted locations, ranging from rou-
crimination, and punitive laws and practices that crimi- tine testing in facilities to community-based outreach.
nalize behaviors and, as a result, limit access to health Despite these achievements, a substantial testing gap
care, including HTS. On November 3, 2020, we searched remains. According to recent estimates, 77% of all peo-
Google scholar, PubMed and the American Medical ple diagnosed with HIV are on ART; however, 40% of
Association website for published research articles
all people with HIV remain undiagnosed.1 Further-
using the terms "Partner Notification Services," "Index
more, despite the annual increases in HIV tests and
Testing," "KP sexual contacts," and "KP social network,"
with no language or date restrictions. Our search turned HIV testing coverage,2 in many settings, HTS is not suf-
up descriptive, retrospective, systematic review, ran- ficiently focused. Many of those at highest risk, such as
domized controlled trials and meta-analysis papers, that partners of people with HIV, young people in high HIV
suggest that testing of biological children and sexual prevalence settings, and key populations (KP) world-
partners utilizing HIV index testing model can be viable wide, remain unreached.
to identify and link children, adolescences and adult KP such as female sex workers (FSW), men who
into care and treatment. have sex with men (MSM), and people who inject drugs
(PWID) are disproportionately affected by HIV. They
Added value of this study comprise approximately 36% of the 1.9 million new
The authors developed a flowchart of the HIV index adult HIV infections that occur each year.1,3 In 2020,
partner testing model among KP, examined partner Key populations, their clients, and sexual partners
notification (PN) delivery techniques, and calculated HIV accounted for 64% of new HIV infections in West and
seropositivity among persons who underwent Index Central Africa, and 25% of new HIV infections in the
partner testing among Key populations in three Niger- East and Southern African subregion.4 Data from Sene-
ian states. Our study analyzed HIV PN delivery models
gal, The Gambia, C^ ote d'Ivoire, Ghana, and Nigeria
selected for 7559 sexual contacts plus injecting partners
of 3119 KP index clients (index partner ratio 1:2.9) who
indicate that a substantial number of infections
accepted index partner testing. Study showed high occur5−8 among MSM, many of whom also report hav-
uptake of the provider assisted notification and referral ing sex with women.9 Based on the 2018 national KP
process for 68.3% index partner testers compared to size estimation carried out by National AIDS, Sexual
the other PN methods. Transmitted Infections Control and Hepatitis Program
(NASCP),10 the total KP in Nigeria is estimated to be
Implications of all the available evidence 720,000. About three-quarters (69%) of the KP have
Including index partner testing as part of a community- been tested for HIV under the national KP program.11
led HTS can help improve HIV case-finding approach for In Nigeria, the prevalence of HIV is on the decline, it
KP, particularly for reaching first-time testers, male KP, dropped from 5.8% in 2001 (ANC Survey report) to
and persons not yet diagnosed with HIV. Results sug- 1.5% in 2018 Nigeria AIDS Indicator and Impact Survey
gest improvements in the rate of HIV testing among (NAIIS). However, KP, including FSW, MSM, and
males through HIV partner notification services. The PWID continue to have a high HIV prevalence. HIV
high enrolment in care and treatment services can be prevalence is respectively 22.9%, 19.4%, and 8.6% in
attributed to a more personal engagement of sexual MSM, brothel-based female sex workers, and non-
and injecting partners by HTS peer-outreach workers at
brothel-based female sex workers.12 In Nigeria, ART
the community level.
coverage in KP is unknown.13−15 KP is understudied
and likely underserved resulting in a limited characteri-
zation of their HIV prevention, treatment, and care
needs.14
are to deliver a diagnosis and effectively facilitate access Although countries are increasing including key
to and uptake of HIV prevention, treatment, and care populations in their national HTS guidelines, imple-
services. Over the past decade, low- and middle-income mentation remains limited, and testing coverage contin-
countries in Africa recorded substantial improvements ues to be low in most settings.2 Poor coverage and low
in the percent of people living with HIV who are aware uptake of HTS among KP are not only related to avail-
of their HIV status from 10% in 2005 to 50% in 2015.1 ability but also the acceptability of services. Low accept-
These achievements have been possible largely because ability frequently reflects unfriendly services, fear of
of the scale-up and use of the wide availability of low- stigma, discrimination, and punitive laws and practices
cost rapid diagnostic tests. The term antiretroviral ther- that criminalize behaviors and, thereby, discourage
apy (ART) is referred to as treatment with drugs that access to health services, including HTS.3 These

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challenges require a new focus and new approaches to Lagos. Under the national KP program, these states
reach people with undiagnosed HIV infection. Many were prioritized for prevention and comprehensive
countries and programs are exploring innovative HIV/AIDS treatment interventions due to the high pop-
approaches, such as index partner testing or partner ulation density and the high number of PLHIV. The
notification services to delivering HTS to achieve Nigerian HIV/AIDS Indicator and Impact Survey has
national and global testing targets. shown that Akwa Ibom has the highest prevalence rate
Index partner testing can be defined as an approach of HIV in the country”. The states of Cross River and
by which a person with confirmed HIV infection (index Lagos were rated 10th and 14th in terms of HIV preva-
case) is asked to contact family members (children, lence rates, respectively”.17 Supplementary 1 is a map of
spouse, sexual partners, siblings, and parents) to see if Nigeria that depicts the study regions and the distribu-
they will accept an HIV test.4 The approach has proven tion of PLHIV throughout the country based on the
to be a key intervention in diagnosing people living with 2019 UNAIDS SPECTRUM HIV estimates. Across sev-
HIV (PLHIV) and enrolling and retaining them in care eral sub-Saharan Africa countries (including Nigeria),
and ART.16 To increase HIV case identification among UNAIDS currently uses routine program data in Spec-
KP, the national KP program funded by the President’s trum software to estimate the national HIV prevalence
Emergency Plan for AIDS Relief (PEPFAR) and imple- and PLHIV burden. The Spectrum package uses the
mented through Non-Governmental Organizations HIV prevalence over time from routine program data or
(NGOs) in Nigeria introduced index partner testing in survey data together with demographic information and
October 2017. All KP patients accessing ART were epidemiological assumptions to model age-specific HIV
encouraged to bring their family members, spouses, prevalence, and incidence and mortality rates, and the
sexual contacts, and/or injecting partners for HIV test- total number of people living with HIV.18 In 2017, the
ing. The national KP program engages directly with KP national HIV program implemented partner HIV
and delivers client-centered services through commu- notification services. The primary source of data for
nity-led programming. HIV testing, prevention, and this study came from Heartland Alliance Nigeria's
care services are provided to KP through differentiated PN activities, which took place between October 1,
service delivery methods, with services delivered in 2018, and September 30, 2019. The 12-month time-
areas where KP may be served without discrimination. frame corresponds to the program cycle timeline or
To build access to services, the national program sup- fiscal year in which program interventions are exe-
ports drop-in centers and personalized outreach, and cuted in Nigeria with technical and financial assis-
alternative pick-up points, such as one-stop-shops that tance from PEPFAR. The national KP program
provide community-based treatment initiation and consists of an integrated HIV prevention and treat-
refills in addition to testing services. ment program that identifies HIV-positive KP in the
We aim to describe the implementation of index community and links them to care and treatment at
partner testing as part of the national KP program and the LGA level.19
to present the first results. We established the HIV sero-
positivity rate among male and female sexual contacts
plus injecting partners of KP index clients and analyzed Definitions of HIV partner notification delivery models
HIV partner notification services and referral services of In this study, partner notification was defined as a vol-
HIV positive index clients. untary process whereby a trained provider asks clients
diagnosed with HIV about their sexual partners and/or
drug-injecting partners, and then, if the HIV-positive
client agrees, the trained provider offers these partners
Methods
HTS. In this study, partner notification was done in two
Study design and setting ways: passive and assisted.20 Under the passive HIV
The study was a retrospective analysis of community-led partner notification services HIV-positive clients were
HIV index partner testing-involving review of secondary encouraged by trained providers to disclose their HIV
data from partner notification services registers. The status to their sexual and/or drug-injecting partners and
registers documented HIV-positive index clients who to suggest HTS to the partner(s) given their potential
were offered partner notification services, and the sexual exposure to HIV infection. Under the assisted HIV part-
and injecting partners elicited. All clients offered part- ner notification services, consenting HIV-positive cli-
ner notification services in the three states were ents were assisted by a trained provider to disclose their
included in this study. Nigeria is organized into 36 fed- status or anonymously notified their sexual and/or
erating states and the Federal Capital Territory which drug-injecting partner(s) of their potential exposure to
hosts the national government. The states are further HIV infection. The trained provider offered HIV testing
sub-divided into 774 Local Government Areas (LGA). to these partner(s). Assisted partner notification was
The cross-sectional retrospective study was conducted done using contract referral, provider referral, or dual
in three focus states Akwa Ibom, Cross River, and referral approaches.

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Contract referral: HIV-positive clients entered a con- on client preferences. Exposed contacts were traced
tract with the trained care providers and agreed to dis- and offered HIV testing.
close their status and the potential HIV exposure to The national KP program is entirely community-
their partner(s) by themselves. According to the con- based, and HIV testing as part of index partner testing
tract, HIV-positive clients are expected to refer their services was offered in nightclubs, hotels, drop-in-cen-
partner(s) to HTS within a specific time. If the partner ters, or community-based ART clinics (One-Stop-Shops
(s) of the HIV-positive individual does not access HTS (OSSs)). Nightclubs and hotels are ideal settings for
or contact the health provider within that period, then HTS interventions, because KP members visit these
the providers contact the partner(s) directly and offered venues to socialize, seek clients, or participate in key
voluntary HTS. population−defining behaviors. In these areas, HIV
Provider referral: With the consent of the HIV-posi- testing was primarily based on the desire or request of
tive clients, the trained provider confidentially contacted the index sexual and/or injecting drug use partners.
the person's partner(s) directly and offers the partner(s) HIV prevention programs for KP are provided through
voluntary HTS. drop-in centers, which are safe places in the commu-
Dual referral: The trained provider accompanied and nity. OSS model for KP established safe spaces in the
provided support to HIV-positive clients that disclosed communities for biological (e.g., HIV testing, sexual
their status and the potential exposure to HIV infection transmission infection (STI) screening), behavioral
to their partner(s). The care provider offered the partner (e.g., risk assessment, peer education) and structural
HTS voluntarily (s). Anonymous techniques in which (e.g., income generating activity) interventions. It inte-
the index case and provider notified the partners of grates differentiated strategies that optimize efficiency
potential exposure without identifying the index part- along the 95−95−95 cascade.21 The project developed
ner's position or engagement standard operating procedures and data-collection tools
(client intake forms, HIV Index Testing Services regis-
ter, or logbook) for use by providers during counseling
Index testing services among key populations in of HIV index patients and meeting their relatives. For
Nigeria contact to be counted under the index testing program,
The national KP program consists of an integrated HIV he/she must be tested for HIV and receive their result
prevention and treatment program that identifies HIV- or be known as HIV positive. The contact could either
positive KP in the community and links them to care self-report a known exposure to someone with HIV as
and treatment at the local government area or commu- their reason for testing, have an index testing referral
nity level. Index testing is also referred to as partner test- letter/card/coupon given to them from their HIV-posi-
ing/PN services. In this approach exposed contacts (i.e., tive partner/family member (client-referral approach),
current, or past sexual partners, and anyone with whom or have been identified during the elicitation process
a needle was shared) of an HIV-positive person (i.e., and contacted through a provider referral. To reduce the
index client), were offered HIV index testing. Every double-counting of index partners and account for re-
newly diagnosed HIV-seropositive becomes an indexing testers in a reporting period, tracking systems with
client from whom to elicit contacts. All index testing “unique identifiers” were established and used to moni-
services meet WHO’s 5C minimum standards, includ- tor the frequency of contact/outreach of a single index
ing consent, counseling, confidentiality, correct test case over time. A unique ID was generated and assigned
results, and connection to HIV prevention (for HIV-pos- to an index partner before HIV testing commences, and
itive and HIV-negative individuals), and linkage to HIV the results collected were entered into an electronic
care and treatment for HIV-positive individuals. Specific database. The partner elicitation process of index testing
program guidelines, tools, and standard operating pro- is a continuous process. Peer navigators followed stan-
cedures were utilized to provide safe and ethical index dard operating procedures to determine when KP was
testing services, in compliance with the WHO consoli- asked again about any new partners or previous part-
dated guideline on partner notification services. To ners that may not have been disclosed previously. Index
reduce the risk of harm, trained providers ensured that testing was assisted by peer navigators. Peer navigators
all index clients got counseling and support services, are KP who were recruited and trained as peer-outreach
such as helplines and screening for Intimate Partner workers to increase demand for tailored HIV services,
Violence (IPV), as per WHO standards. To ensure improve the quality of behavior change communication
compliance with the index testing guidelines, com- and increase access to HIV testing.
munity-based organizations, civil society groups, and HIV testing delivery services to KP in the target com-
networks of key populations conducted community- munities adopted a 2 step HIV rapid testing− serial
led monitoring activities (gather quantitative and algorithm testing strategy. The fourth-generation rapid
qualitative data about HIV services). HIV-positive cli- test kits were used for HIV testing (DetermineTM HIV-1/
ents were offered multiple options for assisted part- 2 Ag/Ab Combo). A non-reactive HIV test result after the
ner notification, and the approach selected was based first test was considered as HIV-negative. A reactive

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result was tested with a second test. When the result and received their results. Previous or known posi-
was reactive again, it was considered HIV-positive and tives are also recorded.
when it was non-reactive it is considered HIV-negative.
HIV testing and counseling, and requests for elicitation
of sexual and injecting partners all take place in a pri- Study population
vate and confidential environment. HIV testing and All contacts (sexual contacts or injecting drug users) of
counseling are available to sexual partners at convenient HIV-positive FSW, MSM, and PWID aged ≥15 years
hours (including nights and weekends) and places who received partner notification services were included
(home, facility, or other community locations). HIV in the analysis. For simplicity, we refer to them as
self-test kits are also provided to clients, which they can “partners” in the rest of the text. The index case's spouse
distribute to their sexual partners. Clients who rejected and casual sex partners are the sexual partners included
HIV testing services were offered the opportunity to be in the study. According to the national KP program,
contacted again after a set length of time. Preventive children under the age of 15 are not classified or named
treatments, such as harm reduction interventions, in any of the KP categories and hence were not included
behavioral interventions, sexual and reproductive health in this study. Only adult KP is enrolled in the care and
interventions, pre-exposure prophylaxis (PrEP), infor- treatment program. Children of KP, on the other hand,
mation on post-exposure prophylaxis, condoms, and are linked to HIV prevention and treatment activities
lubricants, are offered for sexual and injecting contacts through the national HIV program for the general pop-
of clients who test negative. To support HIV treatment ulation. In-person and social network-based HIV testing
and care for HIV positive KP, the national program sup- approaches were used to recruit index clients. KP high-
ports drop-in centers, personalized outreach, and alter- risk networks are used in social network strategies to
native pick-up locations, such as one-stop-shops that refer people for HIV testing. These strategies, which
offer community-based treatment initiation and refills include an enhanced peer outreach strategy, take advan-
in addition to testing services. Multi-month dispensing tage of social, sexual, and drug-using relationships or
for both PrEP and ART are provided and dispensed behaviours to reach high-risk and hidden individuals
through community-based clinics or drop-in centers. who might benefit from HIV testing. The trained care
provider urges KP with HIV or those who are HIV-nega-
tive and at continuing risk of HIV to encourage and
invite others in their sexual, drug injecting, or social net-
Implementation of index testing services works to engage in voluntary HTS as part of the social
Index testing cascade for KP is categorized into four spe- network testing strategy. FSW was defined as women
cific steps based on four program performance indica- who receive money or goods in exchange for sexual serv-
tors. These steps are part of a cascade of ices, and who consciously define those activities as
implementation that begins with an offer of index test- income generating even if they do not consider sex
ing services to the index client (newly diagnosed KP) work as their occupation.22 MSM was defined as (1) self-
and ends in provision of an HIV test to the contacts identification as male and (2) report of oral or anal sex
named by the index client. The steps are: with a man in the prior 12 months.23 PWID was defined
as a person who meets one of the following conditions:
(1) Number of index clients who were offered index (1) self-reporting ever injecting any illicit drug and hav-
testing services. This is the number of index clients ing a visible injection site on the body, (2) self-reporting
(newly diagnosed positive KP) who were offered injecting illicit drugs in the past month.24
index testing services (regardless of whether those
services were accepted by the index client).
Statistical analyses
(2) Number of index clients who accepted index testing We analyzed aggregate-level program data from index
services. This is the number of index clients who testing by counting the number of sexual partners plus
accepted provision of index testing services by a pro- injecting drug users of HIV positive KP who received
vider (including client providing informed consent, HIV index partner testing services between October 1,
acceptance of counseling on index testing, accep- 2018, and September 30, 2019, at the community level.
tance of elicitation of current or past sexual or We conducted four separate analyses: First, we created a
injecting partners and/or partner notification). flow chart diagram of the HIV index testing model from
(3) Number of contacts provided by the index client. three Nigerian states. Second, we utilized proportions to
This is the number of contacts provided by the characterize the methods for HIV partner notification
index client because of accepting index testing serv- of index partners' HIV status and calculated HIV sero-
ices. positivity among those who underwent index testing by
state and KP group. Two proportion Z-test using a 5%
(4) Number of contacts who were tested for HIV. This alpha level (a/2 = 1.96) was used to compare partner
is the number of contacts who were tested for HIV HIV seropositivity by states. The null hypothesis (H0)

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for the test is that the HIV seropositivity across KP Ethics

groups in the study locations is the same. In determin- This analysis was conducted with routine data gathered
ing whether to reject the null hypothesis we used the through the national KP program. Informed consent
method of identifying rejection regions. We rejected the was obtained for all clients who were tested for HIV
null hypothesis when the calculated z-score falls into a through index testing in line with the Nigeria HTS pol-
rejection region. We define the rejection region as an icy. Ethical approval was obtained from the Federal Cap-
area under a normal standard distribution, where the ital Territory, Health Research Ethics Committee,
null hypothesis is not probable. We divided the total Nigeria (approval no: FHREC/2020/01/123/12−11−20).
number of partners of index clients who tested HIV pos- This study only analyzed anonymized and de-identified
itive (numerator: previously known HIV positive data.
testers + newly identified HIV positive) by the total
number of partners who received HIV testing services
to measure the HIV seropositivity. Third, we created a Role of the funding source
dot plot to examine the differences in HIV testing by This research received no specific grant from any fund-
state and sex. Fourth, we constructed a violin chart and ing agency in the public, commercial or not-for-profit
compared the mean HIV seropositivity across the KP sectors. All the authors accept responsibility for the deci-
groups using the One-Way Analysis of Variance sion to submit for publication.
(ANOVA) test and Tukey’s honest significance differ-
ence (HSD) test at 95% family-wise confidence level to
determine whether the differences between the group Results
means of HIV seropositivity are statistically significant, Overview of HIV index testing cascade
and to identify the group means that are statistically dif- Figure 1 shows the cascade of HIV index testing services
ferent from one another. R-software v.4.0.5 was used to and treatment initiation for all KP groups. Of the 10,774
perform the analysis. The authors made sure that the newly diagnosed HIV-positive KP, a total of 10,508
manuscript's structure and flow strictly followed (98%) index clients (5636 FSW, 2805 MSM, and 2067
STROBE guidelines. PWID) were offered index testing services in 54 local

Figure 1. Overview of HIV Testing Services uptake in Index Testing Model from 3 States, Nigeria, October 1, 2018 − September 30,
2019
The flow chart diagram shows how the index partner testing cascade for KP in Nigeria works. The index clients who were offered
index partner testing services are shown by the yellow horizontal bar. The purple bar depicts index clients who accepted to partici-
pate in index partner testing. The index clients' partners who were elicited for HTS are shown by the blue horizontal bars. The elicita-
tion ratio by KP groups is shown by the red boxes. The light green, orange, and grey horizontal bars show how many partners of
index clients were tested for HIV, how many were HIV positive, and how many were on antiretroviral therapy, respectively.

6 www.thelancet.com Vol 43 Month January, 2022

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government areas across the three states during the in FSW and MSM partners (z-test = 9.14, p < 0.00001
study period. Overall, the proportion of index clients and z-test = 17.39, p < 0.00001). HIV seropositivity was
who accepted the services was low, 30% (3119/10,508). also substantially higher in PWID injecting partners
Of n = 3119 KP index clients who accepted the services, than in FSW and MSM partners (z-test = 19.9,
acceptance rate was 42.4% (n = 1322) for FSW, 40.2% p < 0.00001 and z-test = 27.5, p < 0.00001, respec-
for MSM (n = 1255), and 17.4% for PWID (n = 542). A tively). FSW partners similarly had a higher HIV sero-
total of 8989 partners of the 3119 KP index clients were positivity than MSM partners (z-test = 11.4,
elicited for index testing services (index partner ratio= p < 0.00001). Linkage to ART was 93.0% (3492/3753)
1:2.9; 82.8% (n = 7443) male and 17.2% (n = 1546) overall and was above 90% in all subgroups.
female). HIV testing and counseling uptake ranged
from 76.1% (2220/2919) among sexual partners of
FSW to 99.4% (626/630) among injecting partners of Index testing by sex and partner notification delivery
PWID. Testing uptake was 87.0% (3947/4536) among models
MSM and 83.9% (763/909) among sexual partners of HIV testing services differed considerably by sex. About
PWID. Overall, 49.7% (n = 3756) were HIV positive. 79.0% (5999) of males and 21.0% (1546) of female part-
HIV seropositivity rate among partners varied dispro- ners elicited for PN services were tested for HIV.
portionately. It was 37.0% MSM partners, 52.0% for Figure 2 indicates that males made up most of the part-
FSW partners, 71.0% for PWID sexual partners and ners who received HTS (Akwa Ibom 78.7%, Cross river
96.0% for PWID injecting partners. The results of the 73.0%, and Lagos 92.0%). Almost three-quarters
two proportional Z-tests revealed that HIV seropositivity [73.0% (2732/3753)] of those who tested positive were
was significantly higher in PWID sexual partners than males. The majority 84.1% (7556/8989) partners of KP

Figure 2. Dot plot showing differences in HIV testing by state and sex, (October 2018 − September 2019)
The proportion of females and males who obtained HTS in the index partner testing services is shown by the red and blue dots,
respectively. The grey bar depicts the change, and/or difference in HTS distribution by state (vertical axis) and by gender (horizontal
axis).

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index partners who received HIV testing and counseling

services were first-time testers. KP index clients chose
provider referral for 68.3% (5159/7556) of partners, cli-

100.0
30.2
68.2
ent referral for 30.1% (2278/7556), contract referral for

1.1
0.5
%
Overall
1.1% (82/7556), and household/dual referral for 0.5%
(37/7556) of partners respectively (Table 1).

2281
5159

7559
82
37
HIV seropositivity rate and linkage to art by state

n
In Akwa Ibom, 48.2% (3640/7556) of people received
HIV testing and counseling, 32.6% (2462/7556) in

Injecting Partners of PWID

Cross River, and 19.2% (1454/7556) in Lagos (Figure 3).

100.0
HIV seropositivity rate was 89.1% (2194/2462) in Cross

51.9
48.1
0.0
0.0
%
River, 31.9% (1162/3640) in Akwa Ibom and 27.3%
(397/1454) in Lagos (Figure 3). In Cross River, HIV
seropositivity was comparable in PWID injecting part-
ners and PWID sexual partners (99.1%; 581/586 and

325
301

626
98.9%; 433/438) respectively. HIV seropositivity was

0
0
significantly higher in MSM partners (95.6%; 605/633)
than in FSW partners (71.4%; 575/805) in Cross River,
Sexual Partners of PWID
z-test = 13.2, p < 0.00001. In Akwa Ibom HIV seroposi-
tivity was considerably higher in FSW partners (41.3%;

100.0
39.3
57.7
2.9
0.1
566/1371) than in MSM partners (25.2%; 490/1948), z- %
test = 9.8, p < 0.00001. HIV seropositivity among
PWID sexual partners (50.0%; 2/4) and PWID injecting
partners (47.5%; 19/40) in Lagos was not statistically
300
440

763
different, z-test = 0.09, p = 0.928 (Figure 3). The mean
22
n

1
HIV seropositivity was 57.1% among FSW partners,
30.2% among MSM partners, 16.1% among PWID sex-
Sexual Partners of MSM

ual partners, and 11.7% among PWID injecting partners

(Figure 4a). We found a statistically significant differ-
100.0
16.8
81.2
1.2
0.8
%

ence in mean HIV seropositivity by KP type (f(3)=23.07,

p < 0.001). In Figure 4b, The Tukey-HSD test showed
that HIV seropositivity rates among FSW partners were
substantially higher on average than HIV seropositivity
3206

3949

rates among sexual and injecting partners of PWID.

665

46
32

Table 1: Methods for HIV partner notification of index partners HIV status.
n

The mean HIV seropositivity difference between MSM

partners and injecting PWID partners is 18.4, with
MSM partners averaging 18.4 points higher. HIV sero-
Sexual Partners of FSW

positivity was considerably higher among MSM part-

100.0
45.2
54.0
0.63
0.18

ners than among injecting partners of PWID and sexual

%

partners of FSW, respectively. In Lagos, almost all part-

ners were linked to ART. Cross river showed similar
results. Linkage to ART was lower than the UNAIDS-
second 90 goal in Akwa Ibom across FSW, MSM, and
1003
1200

2221
14

PWID sexual partners (Figure 3).

n

Discussion
Partner Notification method

Our study describes the implementation of a commu-

Household/Dual referral

nity-led index partner testing cascade as part of the

Passive/clients referral

national KP program. While the proportion of KP index

Contract referral
Provider referral

clients who accepted PN or index testing services was

low (29.7%), HIV testing uptake among partners of
index clients was high (84.1%). It's worth noting that
Total

there's a scarcity of data on HIV index partner testing

acceptance rates, particularly among KP. According to a

8 www.thelancet.com Vol 43 Month January, 2022

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Figure 3. HIV Cascade of tested index partners by key population group and State, October 2018 − September 2019.
The combo chart shows the HIV testing and treatment cascade for the index partners, disaggregated by state and KP type. The
number of index partners who were tested for HIV (orange) and the number of index partners who were HIV positive is shown in
the graph (grey). The blue line graph depicts the percentage of HIV-positive index partners who were started on antiretroviral ther-
apy, whereas the green bubbles depict HIV positivity rates among index partners according to KP typologies.

retrospective analysis of program data on index partner among MSM in HIV prevention and treatment services
testing cascade among the general population in Zam- in Nigeria.
bia and Kenya, 93% and 98% of PLHIV, respectively, The proportion of the KP index partners tested were
accepted partner notification services.17 Another study mostly males (79%) than females (21%). FSW and
in Lesotho found that 75 percent of index clients who MSM's partners were more likely males, which led to
were offered index partner testing accepted it. When the high number of male partners in our study com-
compared to the acceptability rate reported in the gen- pared to females. Testing uptake among men was there-
eral population, the acceptance rate for index partner fore remarkably higher than in a previous study in
testing was low in our study. KP's continued stigma and Malawi and Rwanda, which found that nearly 70% of
discrimination because of their perceived health status, adult HIV tests reported in 76 low- and middle-income
sexual orientation, and/or gender identity may have countries were among females.15 The approach also
influenced index partner uptake.18 Clients' fear of proved to be effective; half (49.7%) of the successfully
stigma, discrimination, and other human rights viola- referred contacts were found HIV positive, and of these,
tions may explain the low index partner acceptance rate all were newly diagnosed or first-time testers. Available
in our study. According to recent research, fear of evidence suggests that PLHIV are mostly willing to dis-
stigma and criminalization under the Same-Sex Mar- close their HIV status and to participate in provider-
riage Prohibition Act, as well as discrimination against assisted HIV partner notification.27 In our study, part-
KP, are the major reasons for inadequate access to ner notification services were predominantly done
health care and limited participation of KP in national through provider referral (68.3%) compared to client
surveys. The Nigerian government increased the pen- referral (30.1%). A meta-analysis of three individually
alty for homosexuality to 14 years in prison in 2014. randomized trials using all identified partners as the
Anyone who helps gay couples might face a ten-year jail denominator showed that assisted partner notification
sentence.25 These kinds of laws that criminalize homo- services resulted in a 1.5-fold increase in the uptake of
sexuality have forced MSM into hiding, rendering them HTS among partners compared with passive referral.28
more vulnerable to HIV.26 Further studies are recom- These results align with our study which indicated that
mended to determine the immediate effect of this pro- provider referral resulted in a 2.3-fold increase in the
hibitive act on stigma, discrimination, and engagement uptake of HTS among partners compared with the

www.thelancet.com Vol 43 Month January, 2022 9

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Figure 4. Distribution of HIV Seropositivity across KP types, October 2018 − September 2019 (a. top panel) and Tukey-HSD test-95%
family-wise Confidence Level (b. bottom panel).
In Figure 4a, the violin plots show the relationship of KP types to HIV seropositivity. The red dot represents the median, and the
box plot elements show the median HIV seropositivity for injecting partners of PWID is lower than for other KP types. The horizontal
bars in the center represents the interquartile range, and the other points are “outliers” using a method that is a function of the
interquartile range.

passive referral. In a study by Gabriel et al.,29 research- The study found that two-thirds (66.4%) of PLHIV
ers examined the acceptability of anonymous notifica- endorsed provider referral as an acceptable method to
tion by a health service provider (i.e., provider referral) notify their sex partners and nearly three-quarters
in a sample of incarcerated PLHIV, most of whom were (72.4%) endorsed provider referral to notify their drug-
sexually active and using drugs before incarceration. injecting partners. HIV testing uptake among partners

10 www.thelancet.com Vol 43 Month January, 2022

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of index clients elicited for HTS was substantially high likely than women and girls living with HIV to know
in our study (84%). their HIV status, and 27% less likely to be accessing
The 49.7% HIV positivity rate in our study is consis- treatment.41 In western and central Africa, only 25% of
tent with a partner notification study conducted by men living with HIV are accessing treatment.18 When
Nguyen et al.,30 in which the positivity rate among part- people are not on treatment, they are more likely to
ners of index clients was 41.9%. We observed that the transmit HIV. The report also shows that HIV preva-
HIV seropositivity in sexual (71%) and injecting (91%) lence is consistently higher among men within key pop-
partners of PWID was considerably higher than in part- ulations, and outside of eastern and southern Africa,
ners of FSW (71.4%) and partners of MSM (37%). The 60% of all new HIV infections among adults are among
high HIV seropositivity among partners of PWID is in men.
line with the latest UNAIDS 2018 report, which showed Condom usage by sex workers and their clients
that the risk of HIV acquisition among people who varies greatly. In some cases, sex workers have no access
inject drugs was 22 times higher than in the general to condoms, have trouble negotiating their use with cli-
population.31 This risk derives primarily from sharing ents, or are unaware of their importance. The use of
needles and injection equipment but is compounded condoms by sex workers and their clients varies signifi-
through criminalization, marginalization, and poverty. cantly. Sex workers may lack access to condoms, have
The disproportionately high HIV seropositivity among difficulty negotiating their usage with clients, or are
PWID could be linked to the HIV infection dynamics uninformed of their significance. In other situations,
among PWID that suggests overlapping risk groups authorities seize or destroy condoms used by sex work-
with multiple transmission routes. For example, some ers. Physical and sexual assault and harassment of sex
PWID are sex workers, or buy or trade drugs for sex, or workers carrying condoms were revealed in a 2012
are MSM, and may gain HIV through sexual and inject- study in Kenya, South Africa, and Zimbabwe. The fear
ing routes.32 The high seropositivity of HIV among of arrest for condom possession was also being used by
FSW partners compared with MSM partners may indi- police to blackmail and abuse sex workers.42 Emily et al.
cate that sex work and/or transactional sex continues to performed a qualitative study in 2019 to better under-
be the most important cause of new HIV infection in stand the nature and consequences of GBV among
Nigeria.33,34 According to UNAIDS multi-country analy- FSW, MSM, and Transgender women, to influence
sis on new HIV infections by mode of transmission, HIV policy and programming and protect KPs' human
about 10% of new infections are the result of sex work. rights. The study found that emotional and economic
The study indicated that there would be about one and a GBV were the most reported, but that sexual and physi-
half times more new infections due to sex work if it cal GBV, as well as other human rights violations, were
were not for the high levels of condom use reported in reported by about three-quarters of participants.43 GBV
sex worker contacts.35 occurred most often at home, in places where sex work
In Sub-Saharan Africa, it is believed that more than took places such as brothels, bars, and on the street;
half (55%) of all sex workers have HIV.36 Even though public areas such as parks, streets, and public transpor-
sex workers are disproportionately impacted by HIV in tation; health care facilities, police stations; and reli-
every country in East and Southern Africa, HIV preva- gious settings and schools for transgender women and
lence among this community varies widely, ranging MSM. To reduce the national burden of HIV while also
from 5.5 percent in Madagascar to more than 70 percent promoting key populations' human rights, the national
in Lesotho and Uganda. HIV prevalence among sex HIV program implements a variety of diversified pre-
workers in Nigeria was above 30% in 2007.37 There is ventive and treatment package interventions that
no federal or national legislation prohibiting sex work address both HIV and GBV at the community and OSS
in Nigeria. Although sex work is illegal in Nigeria's levels. Modeling estimates in Kenya show that a reduc-
northern states due to Sharia Law. Sex work is legal in tion of approximately 25% of HIV infections among sex
all of Nigeria's Western, Eastern, and Southern states. workers may be achieved when physical or sexual
As a result, in such jurisdictions, police or security serv- violence is reduced.44 In Uganda, a mixed-methods
ices are unable to apprehend sex workers.38 The HIV study investigated the knowledge and attitudes of
positivity rate among FSWs in our research was compa- FSWs and truckers about condom use. Condom
rable to that of countries such as Botswana, Malawi, awareness was high, with 97% of FSWs and 95% of
Rwanda, and Zimbabwe, where more than 40% of truckers agreeing that "using condoms properly and
female sex workers are living with HIV.39 It is estimated regularly decreases the risk of HIV transmission."
that at least 90% of sex workers in East and Southern Condom usage was largely regarded positively, with
Africa are female, although selling sex is also common 91 percent of FSWs and 82 percent of truckers
among men who have sex with men.40 HIV positivity in believing that “condom use is the best means of
our study was higher among males than females. A HIV prevention.” Poverty, male partners' unwilling-
recent report from UNAIDS shows that in sub-Saharan ness to use condoms, alcohol usage before sex, and
Africa, men and boys living with HIV are 20% less perceptions that condoms "kill the mood for sex" are

www.thelancet.com Vol 43 Month January, 2022 11

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all obstacles to regular condom use, according to workers to increase demand for tailored HIV services,
qualitative findings.21 improve the quality of behavior change communication
The national HIV/AIDS program provides targeted and increase access to HIV testing services, the starting
HIV testing services to KP and their high-risk contacts. point of the key population cascade, via social networks.
During the study period, the following HIV testing A key limitation of our study was that program data
modalities were implemented: KP testing in mobile or used for this analysis did not include demographic,
temporary testing locations, such as community cen- socio-economic, and/or clinical characteristics of the
ters, schools, workplaces, hotels, clubs, tents, and vans; study population that could provide more insights into
voluntary counseling and testing which includes testing the study population's risk behavior and the reasons for
in voluntary counseling and testing centers outside of a the variability of HIV seropositivity. We only had quanti-
health facility (i.e., “one-stop shops”), and index partner tative data and did not collect qualitative data that would
testing. According to the national KP program, HIV have helped determine preferred referral strategies by
seropositivity or HIV positivity yield (the percentage of index clients for partner notification. Consequently,
positives found out of those who were tested and other important variables were not available for analysis,
received their test results) varies disproportionately particularly the age of sexual and injecting partners and
across the testing modalities. Overall, HIV positivity the HIV status of serodiscordant couples. The national
yield among KP in our study was 49.7%. According to KP program does not break down HTS or index testing
the national KP program, this was 9.6% in the mobile services by venue, which would have provided informa-
testing modality and 10.7% in the voluntary counseling tion on the proportion of index partner testing done at
and testing modality (see Supplementary 2). These each location. Another limitation was the absence of
results suggest that index testing model can be used to data on viral suppression, which would have given infor-
optimize HIV case identification efforts compared to mation on the status of the last UNAIDS goal.
the other testing models. According to recent research Combining passive and assisted HIV PN services as
in Lesotho, the HIV index testing model had a statisti- part of community-led HTS may help improve HIV
cally significant higher HIV positivity yield among adult case-finding approach for KP and contribute to reaching
clients tested than other HIV testing models (17.6% vs. male partners of KP. Offering partner notification serv-
5.6 percent, p = 0.0009).45 ices from existing community settings (e.g., One-Stop
Provision of partner notification services in the US Shops ART clinics) could greatly expand access to test-
and Europe is safe and effective, as well as cost-effective ing and linkage to care and treatment among people at
for HIV case-finding and linkage to care.46,47 Overall, very high risk of HIV infection, with limited additional
our study shows high ART linkage rate (93.0%) with burden on the health system. Allowing KP index clients
the HIV index testing model. Before the launch of PN to choose their preferred referral method may have
services in 2017, overall linkage to ART among KP was resulted in greater uptake of the referral process, result-
marginally above half (53.7%) in Nigeria. Between Octo- ing in more partners of index clients being elicited for
ber 2017 and September 2019, the linkage to ART HIV testing. Our findings suggest that offering index
increased by thirty-nine percentage points. There is a clients options for passive or provider-facilitated notifi-
remarkably high linkage rate among FSW, MSM, and cation and referral may result in a high uptake of PN
PWID sexual and injecting partners in all states, which services. Further research is needed to evaluate whether
confirms findings from earlier studies in other settings. partner notification strategies, tailored differently, could
Research done in Vietnam to explore assisted partner be more successful in reaching multiple sexual and
notification services as part of community testing serv- injecting partners of KP.
ices for key populations reported that 97.7% of sexual
partners of index clients-initiated ART during the study
period.19 The research done in Kenya and South Africa
Declaration of interests
demonstrated that a family-centered model leads to
In this study, we report no financial or non-financial
more success in finding HIV positives and linking competing interests. OK was supported by a professor-
them to care and treatment.48,49 The high enrolment in ship grant from the Swiss National Science Foundation
care and high uptake of treatment services can be attrib- (Grant no. 163878) and a Swiss National Science Foun-
uted to a more personal engagement of sexual and dation project Grant (320030_192452). All other
injecting partners by HTS providers and peer-outreach authors report no disclosures.
workers at the community level.
A major strength of this study was the large sample
size of 7556 partners from index KP, disaggregated by
FSW, MSM, and PWID. The large sample of KP data Acknowledgments
collected and used in our study compared to other previ- Data used for this study was collected from the Key Pop-
ous studies can be attributed to the peer outreach ulation program in Nigeria through PEPFAR/USAID.
model. In this model, KPs are trained as peer-outreach We thank the staff of Heartland Alliance Nigeria for

12 www.thelancet.com Vol 43 Month January, 2022

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their contribution to data collection and data transmis- 6 Merrigan M, Azeez A, Afolabi B, et al. HIV prevalence and risk
sion from implementation states. behaviours among men having sex with men in Nigeria. Sex Transm
Infect 2011 https://sti.bmj.com/content/87/1/65.
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may be obtained upon request. The 2019 UNAIDS graphics, HIV Knowledge and Risk behaviors, and Prevalence and
Spectrum PLHIV estimates data for Nigeria is publicly Associations of HIV Among Men Who Have Sex With Men in the
accessible and included as a supplement for reference. Gambia November 21. Mary Ann Liebert, Inc., publishers;
2013https://www.liebertpub.com/doi/10.1089/aid.2013.0092.
The code required to replicate the statistical test and 9 Vuylsteke B, Semde G, Sika L, et al. High prevalence of HIV and
analysis would be available upon request to the authors. sexually transmitted infections among male sex workers in Abidjan,
c^ote d'ivoire: need for services tailored to their needs. Sex Transm
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AAO conceived and designed the study and developed Care 2014 https://pubmed.ncbi.nlm.nih.gov/23742663/.
the methodology, principal in data management, did 11 Key population size estimation in Nigeria: novel approaches to sam-
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of the manuscript and provided input into the analysis tory of open access journals. JMIR Public Health Surveill 2021
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https://naca.gov.ng/wp-content/uploads/2016/11/NARHS-Plus-
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script. GE was responsible for data curation and data 14 Larsson EC, Okong P, Thorson A, Ekstr€om AM. Antiretroviral treat-
transmission from program implementation states. OK, ment of HIV in Uganda: a comparison of three different delivery
models in a single hospital. Trans R Soc Trop Med Hyg 2007 https://
AK, AA, and GE reviewed and provided feedback on the www.sciencedirect.com/science/article/pii/S0035920307001447.
final version of the manuscript. Agree with manuscript 15 Demographic patterns of HIV testing uptake in Sub-Saharan ... (n.
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This research received no specific grant from any fund- dom use among female sex workers and truck drivers in Uganda: a
mixed-methods study. Afr Health Sci 2013;13(4):1027–33. https://
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sectors. 18 U.S. National Library of Medicine. Hiv partner notification services.
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19 Decker MR, Wirtz AL, Pretorius C, et al. Estimating the Impact of
Reducing Violence Against Female Sex Workers On HIV Epidemics
Supplementary materials in Kenya and UKRAINE: A Policy Modeling Exercise April 7. Johns
Supplementary material associated with this article can Hopkins University; 2016https://jhu.pure.elsevier.com/en/publica-
be found in the online version at doi:10.1016/j. tions/estimating-the-impact-of-reducing-violence-against-female-
sex-wor-4.
eclinm.2021.101265. 20 Evens E, Lanham M, Santi K, et al. Experiences of gender-based vio-
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