1342
Oral preexposure prophyla
xis uptake, adherence, and
persistence during periconception periods among

women in South Africa

Lynn T. Matthewsa, Manjeetha Jaggernathb, Yolandie Krielb,

Patricia M. Smitha, Jessica E. Habererc, Jared M. Baetend,e,

Craig W. Hendrixf, Norma C. Wareg,h, Pravi Moodleyi,

Melendhran Pillayj, Kara Bennettk, John Basslerl, Christina Psarosm,

Kathleen E. Hurwitzk, David R. Bangsbergn and Jennifer A. Smitb
aDivision of Infect
Child Health Rese
Health Sciences, D
Boston, Massachu
Seattle,Washingto
Maryland, gDepar
Women’s Hospita
National Health L
RWE, Durham, N
Birmingham, Alab
Massachusetts, US

Correspondence t

Tel: +1 (205) 934
Received: 18 Janu

DOI:10.1097/QAD

ISSN 0269-9370 Cop
terms of the Creative
share the work provi
Objective: We developed the Healthy Families-PrEP intervention to support HIV-
prevention during periconception and pregnancy. We evaluated preexposure prophy-
laxis (PrEP) use with three objective measures.

Design: This single-arm intervention study enrolled women in KwaZulu-Natal,
South Africa, who were HIV-uninfected, not pregnant, in a relationship with a partner
with HIV or unknown-serostatus, and with pregnancy plans. PrEP was offered as part of
a comprehensive HIV prevention intervention. Participants were followed for
12months.

Methods: We evaluated periconception PrEP uptake and adherence using quar-
terly plasma tenofovir concentrations. We modeled factors associated with PrEP
uptake and high plasma tenofovir (past day dosing). Patterns of use were
analyzed using electronic pillcap data. Dried blood spots to measure intracel-
lular tenofovir product (past 2months dosing) were analyzed for a subset of
women.

Results: Three hundred thirty women with median age 24 (IQR: 22–27) years enrolled.
Partner HIV-serostatus was unknown by 96% (N¼316); 60% (195) initiated PrEP. High
plasma tenofovir concentrations were seen in 35, 25, 22, and 20% of samples at 3, 6, 9,
and 12months, respectively. Similar adherence was measured by pillcap and dried
blood spots. In adjusted models, lower income, alcohol use, and higher HIV stigma
were associated with high plasma tenofovir. Eleven HIV-seroconversions were
observed (incidence rate: 4.04/100 person-years [95% confidence interval: 2.24–
7.30]). None had detectable plasma tenofovir.
ious Diseases, University of Alabama at Birmingham, Birmingham, Alabama, USA, bMaternal Adolescent and
arch Unit (MRU), Department of Obstetrics and Gynaecology, University of the Witwatersrand, Faculty of
urban, South Africa, cDepartment of Medicine, Massachusetts General Hospital, Harvard Medical School,

setts, dDepartment of Global Health, eDivision of Allergy and Infectious Diseases, University of Washington,
n, fDepartment ofMedicine (Clinical Pharmacology), JohnsHopkins University, School ofMedicine, Baltimore,
tment of Global Health & Social Medicine, Harvard Medical School, hDepartment of Medicine, Brigham and
l, Boston, Massachusetts, iUniversity of KwaZulu-Natal, School of Laboratory Medicine and Medical Sciences,
aboratory Service, jDepartment of Virology, National Health Laboratory Service, Durban, South Africa, kTarget
orth Carolina, lDepartment of Biostatistics, School of Public Health, University of Alabama at Birmingham,
ama, mDepartment of Psychiatry, Behavioural Medicine Program, Massachusetts General Hospital, Boston,
A, and nVinh University College of Health Sciences, Hanoi, Vietnam.

o Lynn T. Matthews, 1900 University Blvd, THT215E, Birmingham, AL 35294, USA.

8148; e-mail: lynnmatthews@uabmc.edu
ary 2024; revised: 1 April 2024; accepted: 8 April 2024.

.0000000000003925

yright Q 2024 The Author(s). Published by Wolters Kluwer Health, Inc. This is an open access article distributed under the
Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and
ded it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

mailto:lynnmatthews@uabmc.edu
http://dx.doi.org/10.1097/QAD.0000000000003925


Preexposure prophylaxis uptake Matthews et al. 1343
Conclusion: The Healthy Families-PrEP intervention supported women in PrEP use.
We observed high interest in periconception PrEP and over one-third adhered to PrEP
in the first quarter; one-fifth were adherent over a year. High HIV incidence
highlights the importance of strategies to reduce HIV incidence among periconception
women.

Clinical Trial Number: NCT03194308
Copyright © 2024 The Author(s). Published by Wolters Kluwer Health, Inc.
AIDS 2024, 38:1342–1354
Keywords: adherence, HIV-Prevention, periconception, perinatal,
pre-exposure prophylaxis, South Africa
Introduction

South Africa is home to nearly 7.5 million people with
HIV (PWH); in 2021, an estimated 130 000 women and
10 000 children acquired HIV [1]. In HIV-endemic
settings, many women conceive a baby with a partner
with HIVor whose serostatus is unknown [2]. For women
who cannot rely on partners to test, engage in care, and
suppress HIV-RNA through antiretroviral treatment,
condomless sex leaves them vulnerable to HIV and thus
increases perinatal transmission risks.

Daily, oral tenofovir disoproxil fumarate/emtricitabine
(TDF/FTC) for preexposure prophylaxis (PrEP) reduces
HIV-acquisition risk, is well tolerated for use among
pregnant and breastfeeding people, and is recommended
by the WHO, U.S. Centers for Disease Control and
Prevention, and South Africa Department of Health for
pregnant and breastfeeding people vulnerable to HIV
infection [3–5]. However, many South Africans,
including pregnant and breastfeeding people, struggle
with adherence [6,7].

Goals to have a healthy baby and remain HIV-free may
motivate HIV prevention during periconception and
pregnancy [8]. Informed by these observations and our
formative work, we developed and tested the Healthy
Families-PrEP (HF-PrEP) intervention to support PrEP
use during periconception and pregnancy periods [9]. This
manuscript describes PrEP use amongwomen planning for
pregnancy in South Africa and participating in the
intervention.We aimed to discover whether women could
be supported to effectively use oral PrEP as a component
of comprehensive HIV-prevention for women intending
to conceive a child while potentially exposed to HIV.
Materials and methods

Study design and population
We conducted a single-arm longitudinal study among
women without HIV in Durban, South Africa.
Participants were planning for pregnancy within the
next year with a partner with HIV or of unknown
serostatus. Data collection occurred from 13 November
2017 to 21 July 2021. Additional eligibility criteria
included female sex; age 18–35 years; not on long-acting
contraception; and likely to be fertile [10]. Women with
pregnancy or HIV at screening were not eligible.
Fieldwork teams recruited women from local healthcare
clinics, gathering spots near the research site, and through
word-of-mouth promotion. Enrolled participants were
offered HIV prevention counseling including TDF/FTC
PrEP with quarterly adherence support and followed for
12months. Objective adherence data were collected from
plasma, whole blood, and electronic pillcaps [9]. This
manuscript is restricted to periconception (the period
from enrollment until study exit or incident pregnancy);
pregnant women were censored for this analysis at the
date of the first positive pregnancy test.

Study activities
HIV prevention counselling (Healthy Families-PrEP)
We developed a counselling intervention, ‘‘Healthy
Families-PrEP’’ (HF-PrEP), to support women in
achieving reproductive goals while minimizing HIV
acquisition, based on South African guidelines and our
formative work [11]. Those initiating PrEP participated
in quarterly adherence support sessions, adapted from
Lifesteps for PrEP [12,13] (Table 1).

Preexposure prophylaxis provision and
monitoring

Dispensing
Women could initiate or discontinue PrEP at any time.
Participants initiating PrEP were provided with a 30-day
supply of PrEP at initiation and a 90-day supply at
subsequent visits.

Clinical laboratory monitoring
Women initiating PrEP completed blood testing to
evaluate renal function and hepatitis B status. Women
with abnormal renal function [serum creatinine >
89mmol/l and estimated glomerular filtration rate
(eGFR) < 60ml/min] or active hepatitis B infection
(hepatitis B surface antigen positive) were instructed to
stop PrEP per WHO guidelines at that time [14].



1344 AIDS 2024, Vol 38 No 9

Table 1. Healthy Families-PrEP support intervention.

Sessionc Activities

1 Rapport building and introduction
Safer conception education a

Motivational strategies to prepare for behavior change
Develop individualized safer conception plan

2 Review prior session content
Safer conception plan review a

Revise plan as needed
Support to implement plan b

3 Review prior session content
Safer conception plan review a

Revise plan as needed
Support to implement plan b

aGuidelines at the time recommend that HIV-uninfected women who
want to conceive a child with a partner with HIV should encourage
partner testing and serostatus disclosurewithin the partnership, encour-
agepartner to initiateART,delay sexwithout condomsuntil heachieves
HIV RNA suppression or is on ART for six months, consider contracep-
tion to delay pregnancy until safer conception strategies are imple-
mented, limit condomless sex to peak fertility, and/or consider sperm
washing, donor sperm, and adoption as alternatives. We also coun-
selled on the availability and benefits of PrEP for HIV prevention.
bMethods employed to support clients to implement plan: education,
problem solving, motivational strategies, communication skills.
cQuarterly adherence support sessions throughout PrEP use. Com-
prehensive counselling was performed by trained study counsellors in
a group format, with the option of one-on-one counseling sessions
based on participant preference and study site logistics.
Participants completed beta-HCG urine testing, indi-
vidual HIV counseling and testing (HCT), and syndromic
screening for sexually transmitted infections (STIs) at
each study visit. Those with pregnancy were eligible to
remain in the study and referred for antenatal care. Those
with STI symptoms were provided with treatment.
Participants who seroconverted were exited from the
study and followed to promote linkage to care. HIV-
RNA samples were sent for genotyping.

Electronic pillcaps
Women accessing PrEP were provided a pill bottle with
an electronic cap (Medication Electronic Monitoring
System (MEMS) [AARDEX, Switzerland]) that recorded
when the device was opened as a proxy for pill ingestion.
Pillcap data were downloaded at each visit and reviewed
with participants.

Adherence-related laboratory evaluation
Women who initiated PrEP provided blood samples at
quarterly visits forwhole blood and plasma.Concentrations
of tenofovir metabolites were assayed in all plasma and a
subset of DBS samples using methods described elsewhere
[15]. The subset of DBS included all HIV seroconversion
samples and a random subset of other samples such that
101 participants (52%) of ever PrEP users were included.

Questionnaires
At enrollment, a questionnaire was administered via face-
to-face interview with a research assistant fluent in
English and the dominant local language to assess
constructs within our conceptual framework for
periconception HIV prevention behavior [16]. Con-
structs were measured using instruments validated in this
setting, described in detail elsewhere [9].

COVID-19 protocol adaptations
The South African government implemented a nation-
wide lockdown from March 27, 2020, through May 1,
2020. The research protocol was temporarily modified to
optimize safety for participants and study staff. In-person
visits were limited to essential visits with telephonic data
collection for other study activities. Once restrictions
were loosened, onsite clinical activities resumed per
original protocol specifications.

Outcomes
The primary outcomes included PrEP uptake defined as
the proportion of participants who ever collected a 30 day
PrEP supply at least once within 12months of enrollment
and PrEP adherence as measured by plasma TFV at the
first quarterly follow-up visit following initiation. Plasma
TFV concentrations at least 40 ng/ml indicate dosing in
the last 24 h (categorized as ‘‘high’’ adherence), between
10 and 40 ng/ml indicate dosing in the prior 3 days
(‘‘moderate’’ adherence), and less than 10 ng/ml indicate
no dosing in the prior 7 days (‘‘low’’ adherence) [17].

We also evaluated adherence using the proportion of days
with a record of pill bottle opening and intraerythrocytic
TFV-DP concentrations, reflecting use over the prior two
months. Pillcap adherence was assessed during active PrEP
follow-up (PrEP initiation through to the earlierof reported
PrEP discontinuation or study exit) and capped at one
opening per day. We estimated mean monthly adherence
over time and the proportion of PrEP initiators with mean
monthly adherence at least 80% (‘‘high’’ adherence) [18].
Intraerythrocyte concentrations of TFV-DP were a
secondary adherence measure for a subset of women. On
the basis of limited data for pregnant or postpartumAfrican
women [19–21], we categorized intraerythrocytic con-
centrations ofmore than 600 fmol/punch, approximately at
least 4 doses per week (‘‘high’’ adherence), 450–600 fmol/
punch as about three doses per week (‘‘moderate’’
adherence), and between 16.6 and less than 450 as less
than three doses per week (‘‘low’’ adherence) [19,22]. We
selected a slightly lower cut-off for the category of ‘‘high’’
basedon the available datawhile accounting forour inability
to adjust for anemia, thrombocytopenia, and BMI [23].

Pillcap data were used to evaluate at least 14-day breaks in
PrEP use followed by resumption of daily use (i.e.
continuation after an interruption) versus 14-day breaks
in PrEP use without resumption (i.e. discontinuation).
We chose 14 days to prioritize interruptions beyond
common-but-transient gaps in pillcap use including
pocket doses (i.e., multiple pills removed for later dosing),
weekend breaks, reduced access to PrEP due to COVID-
19 restrictions, and travel [24].



Preexposure prophylaxis uptake Matthews et al. 1345
Drug concentration and pillcap data were censored at the
last study visit date after the last pillcap opening. If a client
stopped using PrEP in January 2020 and reported this at a
follow-up visit in March 2020, they contributed
adherence data through March and were subsequently
classified as having discontinued PrEP and did not
contribute ongoing adherence data.

Additional outcomes
We assessed HIV incidence (overall and by PrEP initiation
status) measured as the time to first HIV-positive test from
enrollment. Follow-up for incident cases was censored at
themidpoint of the first positive and last negative HIV test
result for infected women. Data for women who did not
acquire HIV was censored at the time of the last available
negative test.

For all participants who seroconverted, Sanger Sequenc-
ing-based HIV resistance genotyping was completed as
described by Manasa et al. [25]. The Stanford University
HIV drug resistance database (version 9.0) was used to
assess the presence of HIV drug resistance mutations and
antiretroviral susceptibilities [26,27]. We defined drug
resistance as having any major drug resistance mutation
(DRM) to nucleoside reverse transcriptase inhibitor
(NRTI), nonnucleoside reverse transcriptase inhibitor
(NNRTI), or protease inhibitors.

Study clinicians monitored adverse events using NIH
DHHS guidelines [28] at all scheduled study visits;
adverse events were reviewed by the DSMB at annual
meetings.

Sample size
We proposed to enroll 350 women [9]. Due to the
COVID-19 pandemic, enrollment was capped at 330 in
March 2020; the last participant enrolled on January
31, 2020.

Statistical analysis
We describe adherence longitudinally with electronic
pillcaps, TFV plasma, and TFV-DP in dried blood spots.
However, our models to predict adherence were
conducted at 3months given high rates of exit due to
seroconversion, pregnancy, losses to follow-up, and less
stable and less representative numbers at 6, 9, and
12months. We used modified Poisson regression with
generalized estimating equations to assess predictors of
PrEP initiation and high adherence (defined as TFV
�40 ng/ml) at the first quarterly visit following PrEP
initiation. Baseline predictors identified based on our
periconception HIV risk conceptual framework [35]
included age, education, household income, number of
prior pregnancies, number of sexual partners, condom
use, tobacco and alcohol use, HIV stigma [16], perceived
HIV risk [29], sexual relationship power [30], dyadic trust
[31], social support [32], and depression [33]. Multivari-
able-adjusted risk ratios were constructed using a change-
in-estimate approach [34] in which relative to a fully
adjusted model (i.e., all known or hypothesized
confounding factors identified by subject matter knowl-
edge of the underlying causal structure included), we
removed, one by one, each factor and recorded the
estimated coefficient for the predictor-outcome associa-
tion. If the removal of the factor changed the coefficient
by at least 10%, it was retained. Missing data are
considered missing at random and complete case analyses
are reported.

All statistical analyses were conducted using SAS software
version 9.4 (SAS Institute, Cary, North Carolina, USA)
and R Statistical Software (v4.1.2; R Core Team 2021).

Ethics and dissemination
The protocol was approved by the Human Research
Ethics Committee at the University of the Witwatersrand
(Pretoria, South Africa), the Institutional Review Boards
of Partners Healthcare (Boston,Massachusetts, USA), and
University of Alabama at Birmingham. The protocol is
registered with the South African Health Products
Regulatory Agency, MCC#20170131) and Clinical-
Trials.gov (NCT03194308). Consent was obtained from
all participants.

Role of the funding source
Study funders did not have a role in study design, data
collection, analysis, interpretation of data, or writing of
this report.
Results

Screening and enrollment
We approached 673 women for screening, of whom 621
completed the screening questionnaire, and 330 met
eligibility criteria and enrolled. Figure 1 summarizes
reasons for ineligibility. Among 330 enrolled women,
four (1%) did not complete safer conception counseling.
Thus, this manuscript reports on data collected from 326
fully enrolled participants. At enrollment, median (25th,
75th percentile) age was 24 (22, 27) years with 279 (86%)
reporting a high school education or beyond and 145
(45%) reporting no prior pregnancies. Most women
(n¼ 287; 88%) reported one sexual partner, and most
(n¼ 313; 97%) did not know the HIV-serostatus of their
desired pregnancy partner. Most (n¼ 205, 70%) reported
that at least one of their sexual partners probably had other
partners (Table 2).

Overall, 189 (58%) women completed all planned follow-
up visits (Fig. 1). The most common reasons for
discontinuing periconception follow-up were pregnancy
(n¼ 56), loss to follow-up (n¼ 46), relocation outside the
catchment area (n¼ 24), and withdrawal of consent
(n¼ 16). Figure 2 illustrates that 312 women (96%)



1346 AIDS 2024, Vol 38 No 9

Fig. 1. Consort diagram. Flow of participants during screening, enrollment, and follow-up.
completed the 3-month follow-up visit and, therefore, all
three primary Healthy Families-PrEP counseling sessions
(Table 1). Eleven women acquired HIV during follow-up.

Preexposure prophylaxis initiation
A total of 195 (60%) women initiated PrEP with most
(n¼ 162; 83%) starting within 2months of enrollment;
97% initiated within 6months of enrollment. In multivar-
iable-adjusted models, participants with higher income,
greater educational attainment, and higher HIV risk
perception were less likely to initiate PrEP during follow-
up (Table 3) (Supplemental File 2 provides unadjusted
associations, http://links.lww.com/QAD/D217).

Preexposure prophylaxis adherence and persistence
Figure 2 highlights summary use at 3, 6, and 9monthswith
all three adherence measures.We found that 86–92% took
at least some PrEP by pillcap, 23–36% by plasma TFV,

http://links.lww.com/QAD/D217


Preexposure prophylaxis uptake Matthews et al. 1347

Table 2. Baseline characteristics, overall and by ever-initiated PrEP.

Overall
(N¼326)

Did not initiate PrEP
(N¼131)

Initiated PrEP
(N¼195)

Individual characteristics
Age, years
Median (IQR) 24 (22, 27) 24 (22, 26) 24 (22, 27)

Education
Grade 7 (Standard 5) - Grade 11 (Standard 9) 47 (14.4%) 14 (10.7%) 33 (16.9%)
Grade 12 (Standard 10) and postgrade 12 279 (85.6%) 117 (89.3%) 162 (83.1%)

Income, monthly ($USD)
< $116 75 (31.6%) 22 (23.4%) 53 (37.1%)
$116–$232 81 (34.2%) 39 (41.5%) 42 (29.4%)
> $232 81 (34.2%) 33 (35.1%) 48 (33.6%)
Missing 89 37 52

Total pregnancies
0 or 1 266 (81.6%) 112 (85.5%) 154 (79.0%)
2þ 60 (18.4%) 19 (14.5%) 41 (21.0%)

Currently using tobacco products
Yes 28 (8.6%) 12 (9.2%) 16 (8.3%)
No 296 (91.4%) 119 (90.8%) 177 (91.7%)
Missing 2 0 2

Frequency of alcohol use in the past year
Never 154 (47.7%) 61 (47.3%) 93 (47.9%)
Any Amount 169 (52.3%) 68 (52.7%) 101 (52.1%)
Missing 3 2 1

Partnership characteristics
Partner HIV Status
Primary partner’s HIV status is known by participant 11 (3.4%) 3 (2.3%) 8 (4.1%)
Primary partner’s HIV status is unknown by participant 313 (96.6%) 127 (97.7%) 186 (95.9%)
Missing 2 1 1

Sexual partners, past 3 months
0 or 1 288 (88.6%) 119 (90.8%) 169 (87.1%)
2þ 37 (11.4%) 12 (9.2%) 25 (12.9%)
Missing 1 0 1

Pregnancy partner (main or other) has other partners
Definitely/Probably does not 90 (30.5%) 41 (33.3%) 49 (28.5%)
Definitely/Probably does 205 (69.5%) 82 (66.7%) 123 (71.5%)
Missing 31 8 23

Depression Score a

� 1.75 303 (94.1%) 120 (92.3%) 183 (95.3%)
> 1.75 19 (5.9%) 10 (7.7%) 9 (4.7%)
Missing 4 1 3

Parenthood motivation: Social control b

Median (IQR) 7 (6, 8) 7 (5, 8) 7 (6, 8)
Missing 8 2 6

HIV Stigma Score c

Median (IQR) 2 (0, 6) 2 (0, 7) 2 (0, 5)
Missing 15 8 7

Perceived HIV Risk d

Median (IQR) 20 (18, 22) 20 (19, 22) 20 (18, 22)
Missing 17 7 10

Sexual Relationship Power Scale e

Median (IQR) 3 (2, 3) 3 (2, 3) 3 (2, 3)
Missing 43 18 25

Dyadic Trust Score f

Median (IQR) 29 (26, 34) 30 (26, 34) 29 (25, 34)
Missing 3 1 2

Social support g

Median (IQR) 4 (4, 4) 4 (4, 4) 4 (4, 4)
Missing 1 0 1

PrEP Optimism h

Median (IQR) 5 (5, 6) 5 (5, 6) 6 (5, 7)
Missing 5 2 3

aDepression: Depression was measured using 10 items questions from the Hopkins Symptoms Checklist [33]. Items were scored on a 4-point Likert
scale [ranging from (1) ‘‘Not at all’’ through (0) ‘‘Extremely’’]. An average score of 1.75 and above was classified as having depression.
bSocial Control: (a) ‘‘My environment (others, family) expect it of me’’; (b) ’’Others around me have children’’; (c) "I want to have a baby to avoid
being an outsider’’.
cHIV stigma: HIV stigma (attributed stigma, perception howmost people feel) was assessed using 17 items from the HIV Stigma Scale [65,66] with
the response profile (1) Agree or (0) Disagree. A score was obtained by summing over the 17 items with higher scores indicating higher attributed
stigma about HIV.



1348 AIDS 2024, Vol 38 No 9

dPerceived HIV risk: Perceived HIV risk was measured using the Perceived Risk of HIV scale developed by Napper et al. [29]. Participants
responded to the seven-item questions with Likert scale responses: (1) ‘‘What is your gut feeling about how likely you are to get infectedwith HIV?’’
[responses range from (1) Extremely unlikely to (4) Extremely likely], (2) ‘‘I worry about getting infected with HIV’’ [responses range from (1) Never
to (4) All the time], (3) ‘‘ Picturingmyself getting HIV is something I find’’[responses range from (1) very hard‘‘ to (4) ‘‘Very easy to do’’], (4) ‘‘Getting
HIV is something I am. . ..’’ [responses range from ‘Not concerned about’ to ‘Extremely concerned about’], (5) ‘‘I am sure I will not get infected with
HIV.’’ [responses range from (1) ‘‘Strongly agree’’ to (4) ‘‘Strongly disagree’’], (6) ‘‘I feel I am unlikely to get infected with HIV.’’ [responses range
from (0) ‘‘Strongly agree’’ through (5) ‘‘Strongly disagree’’], (7) ‘‘I feel vulnerable to HIV infection.’’ [responses range from (5) ‘‘Strongly agree’’
through (0) ‘‘Strongly disagree’’]. Items were summed with higher scores indicating higher perceived HIV risk.
eSexual relationship power: Sexual relationship powerwasmeasured using the Sexual relationship Power Scale [67], which includes 23questions and
two subscales: relationship control [15 questions with response options ranging from (5) ‘‘Strongly agree’’ through (0) ‘‘Strongly disagree’’] and
decision-making dominance subscale [eight questions with response options ‘‘Your partner,’’ ‘‘Both of you equally,’’ or ‘‘You’’]. Items were summed
and overall scorewas derived. A higher score indicatemore power in relationship in the area of relationship control anddecision-making dominance.
fDyadic trust: Dyadic trust was measured using the Dyadic Trust Scale [31], which includes eight-item questions with a 5-point Likert scale
response options [ranging from (4) Agree through (0) Disagree]. An average score was derived with a higher score indicating higher trust.
gSocial support: Social support wasmeasured using 10 items from the Duke-UNC Functional Social Support Questionnaire [32]. Items were scored
on a 4-point Likert scale [ranging from (1) As much as I would like through (4) Never]. An overall score was derived with higher scores indicating
higher social support.
hPrEP optimism: PrEP optimism was assessed based on three-item questions adapted from the Partners PrEP adherence sub-Study [68]: (1) ‘‘PrEP
reduces risk of getting HIV,’’ (2) ‘‘PrEPmakes it easier to relax about sex without condoms,’’ and (3) ‘‘PrEPmakesmeworry less.’’ Responses to each
item questions were given scores of 0 (for ‘‘strongly disagree’’), 1 (for ‘‘disagree’’), 2 (for ‘‘agree’’), 3 (for ‘‘strongly agree’’), and summedwith higher
scores indicating greater PrEP optimism.

Table 2. Continued.
and 49–67% by TFV-DP at 3, 6, 9, and 12months of
follow-up. In addition, 27–43% were highly adherent
taking at least 80% of doses by pillcap, 20–35% with high
plasma tenofovir, and 18–25% with high TFV-DP.
Adherence waned over time by all measures.
Fig. 2. Periconception PrEP use over 12months by electronic pillc
quarter), plasma TFV (past day use), intraerythrocytic TFV-DP (p
Among 180 women who initiated PrEP and had pillcap
data, median duration of persistent PrEP use was 219 days
(range: 1–545). Serial short gaps in use were common;
the median proportion of time on PrEP for PrEP users
was 63% (IQR 43%, 83%). Seventy-eight (43%) women
ap (proportion of days pillcap opened summarized over prior
ast 8weeks use).



Preexposure prophylaxis uptake Matthews et al. 1349

Table 3. Multivariable-adjusted risk ratios and 95% confidence intervals for (a) initiation of PrEP during follow-up and (b) plasma TFV
(>40ng/ml) at 3 months following PrEP initiation.

Outcome: Ever initiated
PrEP during follow-up a

Outcome: Plasma TFV>40
ng/ml at 3 months b

Covariate aRR (95% CI) P aRR (95% CI) P

Age (years) 1.01 (0.97–1.04) 0.74 1.03 (0.96–1.10) 0.46
Education
Grade 7 (Standard 5) - Grade 11 (Standard 9) REF – REF –
Grade 12 (Standard 10) and postgrade 12 0.74 (0.58–0.94) 0.02 1.77 (0.68–4.65) 0.24

Income, monthly ($USD) 0.01 c 0.04 c

< $116 REF REF
$116–$232 0.66 (0.50–0.86) 0.74 (0.37–1.46)
> $232 0.78 (0.62–0.99) 0.44 (0.20–0.98)

Total pregnancies
0 or 1 REF – REF –
2þ 1.18 (0.93–1.50) 0.18 0.91 (0.35–2.37) 0.85

Currently using tobacco products d

No REF –
Yes 0.79 (0.49–1.28) 0.34

Frequency of alcohol use in the past year
Never REF – REF –
Any amount 0.97 (0.81–1.18) 0.78 2.18 (1.20–3.99) 0.01

Sexual partners, past 3 months
0 or 1 REF – REF –
2þ 1.24 (0.96–1.60) 0.10 0.59 (0.17–2.04) 0.40

Pregnancy partner (main or other) has other partners
Definitely/Probably is not REF – REF –
Definitely/Probably is 1.05 (0.84–1.32) 0.66 0.79 (0.39–1.60) 0.52

Depression Score d

� 1.75 REF –
> 1.75 0.71 (0.32–1.60) 0.41

Parenthood motivation: Social control 0.99 (0.92–1.07) 0.86 1.10 (0.92–1.31) 0.30
HIV Stigma Score 1.00 (0.97–1.02) 0.83 1.16 (1.07–1.26) <0.01
Perceived HIV Risk 0.97 (0.94–0.99) 0.046 1.06 (0.96–1.18) 0.23
Sexual Relationship Power Scale 1.04 (0.77–1.41) 0.79 0.87 (0.35–2.15) 0.76
Dyadic Trust Score 1.00 (0.98–1.02) 0.69 1.00 (0.93–1.07) 0.94
Social support 0.89 (0.53–1.48) 0.65 3.29 (0.45–24.18) 0.24
PrEP Optimism 1.00 (0.93–1.07) 0.97 1.12 (0.93–1.35) 0.23

See supplemental file 3, http://links.lww.com/QAD/D218 for each minimally adjusted model of factors associated with initiating PrEP. See
supplemental file 4, http://links.lww.com/QAD/D219 for fully adjustedmultivariable analysis of factors associatedwith ever-PrEP use and 3-month
plasma >40ng/ml.
aPrEP initiation analyses conducted among n¼326 participants who completed all enrollment activities.
bPlasma TFV analyses conducted among n¼134 PrEP initiators who provided a sample at the 3-month follow-up visit.
cP-value computed based on a chi-square distribution with 2 degrees of freedom.
dMultivariable-adjusted analyses for tobacco use and depression score were not conducted due to insufficient sample size.
P-values <0.05 are in bold.
had at least one adherence interruption of 14 days or more
(Fig. 3); median time to first 14-day interruption was 77
(IQR 31–127) days with median time to restart was 22
(IQR 17–40) days. Median time to PrEP discontinuation
without restarting was 200 (IQR 85–326) days (Fig. 4).

Inmultivariable-adjustedmodels, womenwith lower income,
any alcohol use, and higher levels of attributed community
HIV stigma were more likely to have high plasma TFV
concentration (Table 3) (Supplemental File 2 provides
unadjusted associations, http://links.lww.com/QAD/D217).

HIV incidence
Eleven incident infections occurred among 315 partici-
pants with a repeat HIV test result, contributing 272 years
of follow-up. HIV incidence was 4.04 per 100 person-
year [95% confidence interval (95% CI) 2.24–7.30]. Five
of these seroconversions occurred among 122 participants
who did not initiate PrEP with 108 years of follow-up for
an HIV incidence of 4.62 (95% CI: 1.92–11.10). The
remaining six seroconversions occurred among 193
women who initiated PrEP with 164 years of follow-
up with an HIV incidence of 3.66 (95% CI: 1.64–8.15).
Four of the six had undetected plasma TFV at the visit
where theywere diagnosed withHIV. The remaining two
had undetected plasma TFVat the visit prior to diagnosis
with HIV. Three women who had TFV-DP tested had
concentrations below limits of detection. Two additional
women had either undetected of a low concentration
(21.3 fmol/punch) at a visit prior to HIV-seroconversion.
Among the six women who initiated PrEP and
seroconverted, three had NNRTI resistance mutations
(V106M, K103N, E138A), all unrelated to exposure
study product (TDF/FTC).

http://links.lww.com/QAD/D217
http://links.lww.com/QAD/D218
http://links.lww.com/QAD/D219


1350 AIDS 2024, Vol 38 No 9

Fig. 3. Proportion ofNU180 periconception participants who started PrEP and used the electronic pillcap who had adherence
gaps of 1 through >–14days.
Adverse events
We observed 60 adverse events (among 44 participants) of
which 23 events (among 20 participants) were considered
serious. None of the serious adverse events were deemed
to be related to study procedures, including PrEP use
Fig. 4. Time toPrEPdiscontinuation (black) and95%CI (grey),wher
in treatment without resumption (based on pillcap data) among N
(See Supplemental file 1 for all adverse events, http://
links.lww.com/QAD/D216). No clients were advised to
stop PrEP due to renal dysfunction. One unvaccinated
person with HBV at baseline stopped PrEP shortly
after initiation.
ePrEPdiscontinuation is definedas thefirst 14-day interruption
U180 periconception participants who initiated PrEP.

http://links.lww.com/QAD/D216
http://links.lww.com/QAD/D216


Preexposure prophylaxis uptake Matthews et al. 1351
Discussion

We conducted a longitudinal study offering an HIV
prevention intervention, Healthy Families-PrEP, to
women planning for pregnancy in an urban South
African setting with one of the highest HIV prevalence
rates in the world. The majority of participants did not
know their partner’s status, suspected he had other
partners, and were engaging in condomless sex with goals
to have a child. The HF-PrEP intervention supported
high PrEP uptake (60%) and high adherence over
3months for 20–43% of participants (depending on the
adherence measure used). By pillcap, most women had
gaps in their PrEP use with a median time to
discontinuation of 199 days. We observed high HIV
incidence and the findings suggest the importance and
value of programming to promote HIV prevention for
women planning for pregnancy. PrEP interest is high, and
many women need additional adherence support and/or
alternative prevention strategies.

Our findings of high adherence compared to many other
demonstration projects among cisgender women suggest
the value of PrEP care for this population. In a recent
analysis of more than 6000 cisgender women accessing
TDF/FTCPrEP in demonstration projects, including 78%
African women, only 17% were highly adherent to PrEP
by intracellular tenofovir concentrations [6]. Others also
observed goals to have a healthy baby and remainHIV-free
can motivate HIV prevention. In a U.S. study conducted
among women without HIV planning pregnancy with
menwithHIV, 87% took at least four PrEP doses perweek,
by intracellular TFV-DP [35]. In Kenya, a periconception
HIV prevention study among HIV-serodifferent couples
observed that 81%of partnerswithoutHIV tookmore than
80% of PrEP doses [36]. We implemented an intervention
similar to that used in the current study in Uganda and
observedTFV-DPconcentrations corresponding to at least
four doses among 41% of women at 6-month follow-up
[37]. These data highlight the importance of integrating
HIV prevention counseling, including PrEP, into precon-
ception care to reduce HIV incidence among women and
infants. In addition, as more products are approved, choice
of delivery method (vaginal ring, injectable, oral) may
support uptake and adherence [38]. Novel longer-acting
PrEP drugs such as the dapivirine (DPV) vaginal ring and
injectable cabotegravir are efficacious [39–41], approved
for use in South Africa [42,43], andmay serve as important
PrEP options for women who struggle with daily oral
medications. Indeed, emerging data suggest that PrEP
choice may promote use [44,45]. Understanding safety
profiles and securing approval for use in women planning
for and with pregnancy will be important [46–49].

The intervention supported about a third of women to use
daily oral PrEP well enough to be protected from HIV
based on pharmacokinetic estimates [18–21]. On the basis
of real-world PrEP use, more women had some protection
by taking more than two doses per week [6]. ALthough
HF-PrEP worked for many women, it did not help all
participants to successfully use PrEP. We observed an
association of poorer adherence associated with lower
perceived community HIV stigma. Women perceiving
higher community levels of stigma may have experienced
increased motivations to use PrEP and avoid HIV. We also
observed higher adherence with alcohol use and lower
income; generally, in the literature, womenwith competing
demands (e.g., lower income, alcohol use [50,51]) struggle
with adherence. Perhaps in this context, women faced
other challenges that encouraged them to engage in their
HIV prevention strategy; this positive association with
alcohol use was also observed among pregnant women
accessing PrEP in Cape Town [52] and men accessing PrEP
in rural KwaZulu-Natal [53], suggesting that alcohol use
should not be a contra-indication to PrEP care. In a nested
qualitative substudy, women in our cohort described
challenges getting to study visits (including for refills),
succeeded when they were able to disclose PrEP use to a
supporter, and made decisions about PrEP use based on
sexual activity [24]. Additional intervention content could
add PrEP modality choice, community delivery options,
leverage problem solving to support PrEP use disclosure,
and adapt to provide women with the counseling they need
when they need it [54].

Interpretation of our data varies by the adherence
measure used and degree to which a given adherence
threshold correlates with PrEP effectiveness. Differences
observed across the three PrEP adherence measures in this
cohort highlight the value of incorporating multiple
measures and expose gaps in our understandings of
tenofovir pharmacokinetics for cis-gender women. High
adherence by electronic device waned whereas the
proportion with high concentrations by plasma and
whole blood measures were relatively stable, suggesting
that motivations to use the pillcap due to social desirability
bias may have been present and waned over time [55].
However, our limited understandings of how to interpret
pharmacokinetics for cis-gender black women may also
underestimate adherence [56]. We rely on the pillcap data
to evaluate stops and starts, which are common and
important to understanding PrEP use. On the basis of our
paired pillcap and drug concentration data, the pillcaps
may be insensitive for capturing gaps.

Importantly, we observed high HIV incidence in this
population of women planning for pregnancy. HIV
acquisition during pregnancy and breastfeeding contrib-
utes to about one-third of childhood HIV incidence [57].
In this study, the first to our knowledge to measure
periconception HIV acquisition risk longitudinally in an
HIV-endemic setting, we observed an HIV incidence of
4.04 per 100 person-years (95% CI: 2.24–7.30),
highlighting the importance of developing effective
prevention programs for this population. This finding
highlights the importance of offering PrEP to women



1352 AIDS 2024, Vol 38 No 9
independent of whether their partner has been diagnosed
and disclosed serostatus. One-third of men with HIV
(MWH) in South Africa do not know their serostatus [58],
and less than half of women are aware of their partner’s
serostatus [59,60]. Interventions to promote knowledge of
partner serostatus remain important, but should not
undermine opportunities to provide PrEP to women who
may not know their partner’s serostatus but live in an HIV-
endemic area or otherwise feel vulnerable to HIV [48].
Educating men about HIV-prevention options for their
pregnancy partners may also support uptake [61].
Reassuringly, genotyping of the virus among those with
seroconversion revealed mutations that are not associated
with exposure to NRTIs (e.g., tenofovir, emtricitabine)
and thus are likely to represent transmitted resistance [62].

This project was conducted prior to approval of TDF/
FTC as PrEP for women planning for or with pregnancy
in South Africa, thus subject to regulations for
investigational drug. Accordingly, we collected detailed
information on adverse events. We observed a reassuring
safety profile consistent with many PrEP studies [63,64].

Strengths of this study include incorporation of multiple
adherence measures over time among a rarely studied
population of women vulnerable to acquiring HIV.
Limitations include that this was a research study, thus
adherence may have been higher than among the general
population. The project was conducted when TDF/FTC
was not recommended for people planning for pregnancy
in South Africa, which may have compromised use.
Conclusion

Our findings support the importance of HIV prevention
for women planning for pregnancy in HIV endemic
settings. Female-controlled prevention strategies are
critical, and oral PrEP is an important component of
safer conception care which women choose to use. Our
adapted intervention helped support about a quarter of
women to use PrEP well with closer to 50% using PrEP
well enough to secure some protection.
Acknowledgements

Lynn T. Matthews – involved in all aspects.

Manjeetha Jaggernath – protocol development, data
collection, data cleaning, analysis interpretation.

Yolandie Kriel – protocol development, data collection,
data cleaning, analysis interpretation, manuscript writing.

Patricia Smith – data collection, management, writing.

Jessica E. Haberer – protocol development, adherence
measurement interpretation.
Jared Baeten, Craig Hendrix – protocol development.

Norma C. Ware – protocol development (qualitative).

Pravi Moodley, Melendhran Pillay – data generation,
analysis, writing.

Kara Bennett, John Bassler – analysis.

Christina Psaros – protocol development, adherence
counseling support.

Kathleen Wirth Hurwitz – protocol development,
analysis.

David R. Bangsberg – protocol development.

Jennifer A. Smit – all aspects.

The authors would like to thank our participants, the
National Institutes of Mental Health and Gilead Sciences
for their support of operations, and all other team
members who made this project possible.

The data that supports the findings of this study are
available in the supplementary material of this article.

This work was supported by the National Institutes
of Mental Health [www.nimh.nih.gov; Awards:
NIMHK23MH095655 and NIMHR01MH108412; PI:
LTM]. Gilead Sciences (www.gilead.com) provided
Truvada (TDF/FTC) as PrEP and supported operations.
The funders had no role in study design, data collection
and analysis, decision to publish, or preparation of
the manuscript.

Conflicts of interest
Dr Matthews received operational support from Gilead
Sciences.

Dr Haberer has been a consultant for Merck and owns
stock in Natera.

Dr Hurwitz and Ms. Bennett are employed by and own
equity in Target RWE, which has received fees from
Amgen, Baxter International, Gilead Sciences, Janssen
Research & Development (Janssen R&D), and Merck
outside the submitted work.

Dr Baeten is an employee of Gilead Sciences, outside of
the present work.

Dr Hendrix has received research funding from Gilead
Sciences and Merck and is founder and a nonfiduciary
manager of Prionde Biopharma, LLC, outside of the
present work. There are no conflicts of interest for the
remaining authors.

http://www.nimh.nih.gov/
http://www.gilead.com/


Preexposure prophylaxis uptake Matthews et al. 1353
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	Temporal changes in the relative frequency of K103N variants in plasma�RNA
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	Temporal changes in the relative frequency of K103N variants in plasma�RNA
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	Temporal changes in the relative frequency of K103N variants in plasma�RNA
	Temporal changes in the relative frequency of K103N variants in plasma�RNA

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	Temporal changes in the relative frequency of K103N variants in plasma�RNA
	Temporal changes in the relative frequency of K103N variants in plasma�RNA
	Temporal changes in the relative frequency of K103N variants in plasma�RNA
	Temporal changes in the relative frequency of K103N variants in plasma�RNA
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	Temporal changes in the relative frequency of K103N variants in plasma�RNA
	Temporal changes in the relative frequency of K103N variants in plasma�RNA
	Temporal changes in the relative frequency of K103N variants in plasma�RNA