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- 1. EPIDEMIOLOGY
Predictors of Attempted Suicide Among Youth Living With
Perinatal HIV Infection and Perinatal HIV-Exposed
Uninfected Counterparts
Philip Kreniske, PhD,a
Claude Ann Mellins, PhD,a
Curtis Dolezal, PhD,a
Corey Morrison, BA,a
Eileen Shea, MPH,b
Prudence W. Fisher, PhD,c
Luke Kluisza, MS,a
Reuben N. Robbins, PhD,a
Nadia Nguyen, PhD,a
Cheng-Shiun Leu, PhD,a,d
Andrew Wiznia, MD,e
and Elaine J. Abrams, MDf
Background: Suicide is a leading cause of death among adoles-
cents and young adults (AYA). AYA living with perinatally acquired
HIV infection (AYALPHIV) are at higher risk of attempted suicide
when compared with AYA who were perinatally HIV-exposed but
uninfected (AYAPHEU). To inform interventions, we identified risk
and protective factors of attempted suicide among AYALPHIV
and AYAPHEU.
Setting: Data were obtained from a longitudinal New York
City–based study of AYALPHIV and AYAPHEU (n = 339;
enrollment age 9–16 years) interviewed approximately every
12–18 months.
Method: Our main outcome was suicide attempt at any follow-up.
The DISC was used to assess psychiatric disorder diagnoses and
attempted suicide and the Child Depression Inventory to assess
depressive symptoms. Psychosocial and sociodemographic risk
factors were also measured. Analyses used backward stepwise
logistic regression modeling.
Results: At enrollment, 51% was female individuals, 49% Black,
40% Latinx, and 11% both Black and Latinx. Attempted suicide
prevalence was significantly higher among AYALPHIV compared
with AYAPHEU (27% vs 16%, P = 0.019), with AYALPHIV
having 2.21 times the odds of making an attempt [95% confidence
interval: (1.18 to 4.12), P = 0.013]. Higher Child Depression
Inventory scores were associated with an increased risk of attempted
suicide in both groups and the total sample. The presence of DISC-
defined behavior disorder increased the risk of attempted suicide in
the total sample and the AYALPHIV subgroup. Religiosity was
protective of attempted suicide in AYALPHIV.
Conclusions: AYALPHIV had increased suicide attempts com-
pared with AYAPHEU. Religiosity was protective in AYALPHIV.
Highlighting a need for prevention, early mental health challenges
were associated with risk.
Key Words: adolescence, young adult, HIV, mental health, suicide,
attempted suicide
(J Acquir Immune Defic Syndr 2021;88:348–355)
Suicide is the second leading cause of death among
adolescents and young adults (AYA) in the United
States.1 Between 2007 and 2015, rates of attempted suicide
doubled among 5- to 18-year-olds,2 and death by suicide
paralleled this increase.3 History of attempted suicide is a
strong predictor of eventual death by suicide.4–6 Moreover,
youth with chronic health conditions have 3.5 times the odds
of attempting suicide compared with healthy peers.7 Given
advances in antiretroviral treatment, HIV is now considered a
chronic health condition, and an estimated 1.7 million
children aged younger than 15 years living with HIV globally
are likely to survive into adolescence and young adulthood—
a time when suicide risk increases dramatically.8 Our pre-
vious research suggests that AYA living with perinatally
acquired HIV (AYALPHIV) had more than twice the odds of
ever attempting suicide when compared with AYA who were
perinatally HIV-exposed but uninfected (AYAPHEU).9
In the early years of the HIV epidemic, researchers
identified high rates of suicide among AYA living with
behaviorally acquired HIV.10,11 With the introduction of
effective antiretroviral therapy (ART), some studies noted a
substantial decrease in suicide among people living with
HIV12 (PLHIV), yet others found suicide among PLHIV
elevated when compared with the general population.13 A
recent systematic review and meta-analysis suggests risk of
suicidal death is 100-fold higher among PLHIV with the risk
Received for publication February 18, 2021; accepted July 22, 2021.
From the a
HIV Center for Clinical and Behavioral Studies, New York State
Psychiatric Institute and Columbia University, New York, NY; b
Depart-
ment of Psychiatry, Mental Health Data Science, Columbia University
Medical Center, New York, NY; c
Child and Adolescent Psychiatry, New
York State Psychiatric Institute and Columbia University, New York, NY;
d
Department of Biostatistics, Mailman School of Public Health, Columbia
University, New York, NY; e
Jacobi Medical Center, Albert Einstein
College of Medicine, New York, NY; and f
ICAP at Columbia University,
Mailman School of Public Health and Vagelos College of Physicians &
Surgeons, Columbia University, New York, NY.
Supported by the National Institute of Mental Health (R01MH06913 PI
Mellins and P30MH43520 PI Remien). P.K. was also supported by
K01MH122319 (PI Kreniske) and T32MH019139 (PI Sandfort) and a
New York State Office of Mental Health Policy Scholar Award. The
funders had no role in study design, data collection and analysis, decision
to publish, or preparation of the manuscript.
The authors have no funding or conflicts of interest to disclose.
Correspondence to: Philip Kreniske, PhD, HIV Center for Clinical and
Behavioral Studies, New York State Psychiatric Institute and Columbia
University, 1051 Riverside Drive, New York, NY 10032 (e-mail:
pk2361@cumc.columbia.edu).
Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved.
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- 2. directly associated with HIV progression.14 Despite the
introduction of ART, AYA living with HIV (AYALHIV)
may face challenges in developing peer relationships15–17 and
are at increased risk of depression and anxiety.18–20 Although
these are known risk factors of suicide in HIV-negative
adolescents, a recent systematic review noted few longitudi-
nal studies and few studies with comparison groups that
examined suicidality among AYALHIV.18
One of the few studies to examine correlates of
suicidality among AYALPHIV found AYA depression,
conduct disorder, and having a caregiver with mental health
problems were all associated with an increased risk of suicidal
behavior, whereas child-reported “good parenting” was pro-
tective.21 However, the study was cross-sectional and
observed risk of suicidality at only one time point, making
it difficult to determine causal priority of study variables.
Another study in the United Kingdom among AYALPHIV
and peers who were affected by HIV did not identify
differences in self-harm, yet both groups had lower self-
esteem when compared with findings from a national survey
of adolescents.22
It is well established that mental health disorders,
including depression and anxiety, increase the risk of suicidal
thoughts and behaviors among AYA23–28 and
AYALHIV.21,29–31 Furthermore, AYALHIV have higher
prevalence of mental health disorders, including depression,
anxiety, and conduct problems, compared with HIV-negative
AYA.18,19,32,33 Thus, given the higher prevalence of this
known risk factor, and the few existing longitudinal studies,
an examination of suicidality among AYALHIV is warranted.
Beyond mental health, research mostly among HIV-
negative adolescents suggests that a range of sociodemo-
graphic factors can also affect suicidality.23,34 For example,
more young women than young men report suicidal ideation,
yet mortality from suicide is typically higher for young men,
and lesbian, gay, bisexual, transgender, and questioning youth
show elevated prevalence of attempted suicide when com-
pared with heterosexual youth.23,35–37 Racial and ethnic
differences in suicidality have also been identified and
attributed partly to the impact of discrimination, mental
health stigma, and cultural distrust of providers.23,34,38–41
Of particular relevance to this study, a nationally representa-
tive sample from 1991 to 2017 showed Black AYA having a
significant linear increase in suicide attempts over time,
whereas AYA of other racial groups experienced significant
linear decreases.41
Given the staggering number of AYA affected by HIV
globally, there is a significant need to understand predictors of
suicidality to inform preventive interventions. The objective
of this study was to examine a range of early-adolescent
psychosocial and sociodemographic predictors of attempted
suicide throughout adolescence and young adulthood in a
longitudinal cohort study of predominately Black and Latinx
AYALPHIV with a comparison group of AYAPHEU.
Theories of suicidality have long recognized the importance
of considering psychological, social, and structural factors
when assessing suicide risk.11,42–44 This study was informed
by Social Action Theory45 that considers risk and protective
factors from individual, social, and contextual domains, with
mental health as an outcome. This secondary analysis
considers suicide attempt as the specific mental health
outcome and builds on our earlier work by including 2
additional survey rounds and examining predictors of
attempted suicide among the cohort and within AYALPHIV
and AYAPHEU groups, thus extending the fields understand-
ing of suicide risk and protective factors of young people
affected by HIV.
METHOD
Study Population
The Child and Adolescent Self-Awareness and Health
study (CASAH) is an ongoing longitudinal cohort study
(N = 339) of AYALPHIV (n = 206) and AYAPHEU
(n = 133). AYALPHIV and AYAPHEU aged 9–16 years
were recruited from 4 New York City (NYC) medical centers
between 2003 and 2008. Inclusion criteria at enrollment were
perinatal HIV exposure; cognitive capacity to complete the
interview; English-speaking or Spanish-speaking; and care-
giver with legal capacity to sign consent for adolescent
participation. Providers identified eligible patients in their
clinics and referred interested caregivers and adolescents to
the study. Participants and caregivers completed a psychoso-
cial battery at enrollment with follow-ups every 18 months
(CASAH2; 2008–2013; CASAH3; 2013–2018). To date, 7
follow-up (FU) interviews have been conducted. Interviews
were administered in participants’ homes, over the phone, at
clinics, or in the CASAH offices by trained research
assistants. Participants were compensated for travel expenses
and time. The study was approved by the Columbia
University/New York State Psychiatric Institute Institutional
Review Board. Caregivers and adolescents aged 18 years or
older provided written informed consent. AYA younger than
18 years provided written assent, and caregivers gave written
informed permission for youth participation. At FU5, AYA
provided written consent for interviews and collection of data
from their medical providers.
Study Measures
Social Action Theory 45 that includes individual, social,
and contextual domains informed the selection of domains that
were included in the larger CASAH interview battery. For this
analysis, we selected risk and protective factors that were
identified through a review of adolescent HIV, suicidality, and
mental health literature4,7,9,18,21,23,25–31,34–36,38–40,46–51 from the
CASAH battery. These sociodemographic and psychosocial
measures were gathered at enrollment, and suicidality was
measured at enrollment, FU1, FU2, FU4, FU5, and FU7.
Suicidality
Suicidality was assessed using the DISC.52 Participants
were asked, “Have you ever in your whole life tried to kill
yourself or make a suicide attempt?” A dichotomous variable
was created to identify participants who reported at least one
suicide attempt at any of the 5 FUs after enrollment. We
HIV-Exposed But Uninfected Counterparts
J Acquir Immune Defic Syndr Volume 88, Number 4, December 1, 2021
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- 3. recorded the earliest age that a participant reported a suicide
attempt. All participants who reported a suicide attempt or
suicidality were evaluated for active suicidal ideation and
were offered mental health referrals in accordance with
CASAH’s emergency protocol. No participants needed to
be taken to the emergency room at the time of the interview
for active suicidal ideation.
Sociodemographics
Demographic variables at enrollment included sex
(female/male), age (measured continuously), sexual orienta-
tion (heterosexual/not), perinatal HIV status (positive/
negative), and race/ethnicity (Black, Latinx, Black and
Latinx, or neither Black nor Latinx). Because all participants
in the final models were Black, Latinx, or Black and Latinx,
we created a three-level race/ethnicity variable (Black, Latinx,
and Black and Latinx).
Psychiatric Disorders
For this analysis, we used psychiatric disorders assessed
with the DISC53 at enrollment. This structured diagnostic
instrument asks participants about symptoms experienced in
the past year for the most common psychiatric diagnoses and
strictly adheres to the rules promulgated by DSM for
assigning diagnosis. For example, for major depressions,
individual criteria have to be present most of the day, nearly
everyday; for attention deficit hyperactivity disorder, each
symptom must be present for a duration of 6 months. The
following diagnoses were examined: mood disorders (major
depression, dysthymia, mania, and hypomania); anxiety
disorders (social phobia, separation anxiety, specific phobia,
panic, agoraphobia, generalized anxiety, and
obsessive–compulsive); and behavior disorders (attention
deficit hyperactivity disorder, oppositional defiant, and con-
duct). Given the low prevalence for individual disorders, we
examined dichotomized categories (yes/no): any mood dis-
order, any behavior disorder, and any anxiety disorder.
Depressive Symptoms
Because young adolescents may not yet meet full
criteria for major depression yet have significant symptoms,
a key predictor of suicidality, we also assessed symptoms of
depression using the Child Depression Inventory (CDI),54 an
instrument composed of 27 items rated on a 3-point scale
[from 0 (none) to 2 (distinct symptom)]. The total CDI score
(0–54) was used for these analyses, with higher scores
indicating higher severity of depressive symptoms
at enrollment.
Young Adult Life Events
We used items from a Life Events Checklist developed
by one of the authors (C.A.M.) and providers at a pediatric
HIV mental health program.55 The Life Events Checklist,
consisting of 43 items, asks participants whether they have
experienced various life stressors in the past year (yes/no) and
whether the effects of these events were “good,” “neutral,” or
“bad.”56 For these analyses, a subscore was created from a
subset of 18 particularly stressful items typically considered
adverse childhood experiences57 as possible relevant predic-
tors of suicidality (eg, parents divorced, death of a family
member). Responses were scored for both the total measure
and subscore measure, with higher scores indicative of having
experienced more adverse life events at enrollment.
City Stress Inventory
The City Stress Inventory is a 16-item questionnaire
used to measure perceived neighborhood stress, with partic-
ular attention paid to urban stressful situations that AYA may
experience in their neighborhoods at enrollment.58 AYA
reported how frequently they experienced stressful events
(eg, seeing drug deals; witnessing gang violence) in their
neighborhood in the past year using a 4-point scale [from
0 (never) to 4 (often)]. Higher scores indicated a higher level
of neighborhood stress.
Religiosity
A modified version of the Systems of Belief Inven-
tory,59 a 15-item instrument, was used to assess religiosity at
enrollment. Participants reported their religious affiliation,
frequency of participation in religious activities, belief in a
higher order, and the importance of religion or spirituality in
their life. The total scores of these items ranged from 0 to 18,
with higher scores indicating higher religiosity.
Self-Concept
Self-concept was measured at enrollment using the
Tennessee Self-Concept Scale:2 (TSCS:2).60 The scale is
composed of self-descriptive items that are answered on a 5-
point Likert scale ranging from 0 (not at all) to 5 (very much).
Items are organized according to 4 subdomains: personal self-
concept (eg, “I’m a cheerful person”), family self-concept (eg,
“I am a member of a happy family”), social self-concept (eg,
“I am a friendly person”), and academic self-concept (eg, “I
know as much as the other children in my class”). Subdomain
scores were used for these analyses, with higher scores
indicating better self-concept in those areas.
Social Problem-Solving
The Social Problem-Solving Inventory for Adoles-
cents,61 a 25-item instrument, was administered at enrollment
to assess affective, cognitive, or behavioral responses to real-
life problem-solving situations. Participants rated statements
(eg, “I believe my problems can be solved”) on a 5-point
scale, ranging from 0 (not at all true of me) to 4 (extremely
true of me). Total scores were calculated, with higher scores
reflecting better problem-solving ability.
Kreniske et al J Acquir Immune Defic Syndr Volume 88, Number 4, December 1, 2021
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- 4. ART Adherence
For AYALPHIV, ART adherence was measured using
a single, validated self-report item from the pediatric ACTG
study.62 Both AYA and caregivers were asked when the AYA
last missed an ART dose (within the past week, 1 month ago,
2–3 months ago, .3 months ago, and never). Responses were
dichotomized based on whether AYA missed an ART dose in
the past month (yes vs no).
HIV Stigma
Stigma among AYALPHIV was assessed using the
Social Impact scale at enrollment.63 Using a 4-point Likert
scale, participants reported how much they agreed with
statements concerning social rejection, isolation, and inter-
nalized shame related to their HIV status (eg, “I feel I need to
keep my HIV a secret”). Scores were calculated from
participant responses, with higher scores indicating higher
levels of perceived HIV-related stigma.
Statistical Analysis
Descriptive statistics were calculated and AYALPHIV
and AYAPHEU participants were compared on enrollment
demographic and psychosocial variables. The t tests were
used to compare the 2 groups for continuous variables. For
dichotomous variables, the x2 tests or in the case of low
expected cell counts (eg, mood disorder variable), the Fisher
exact test were used.
Backward stepwise logistic regressions were conducted
predicting attempted suicide with enrollment demographic
and psychosocial variables. All independent variables were
entered in the model and then variables not significantly
associated with suicide attempt were removed one at a time
until only significant predictors remained (P # 0.05). The
regressions were run separately for the overall group, for
AYALPHIV, and for AYAPHEU. Independent variables
were the same in each case, except the AYALPHIV model
included ART adherence and HIV stigma.
RESULTS
At enrollment, participants included 339 youth (206
PHIV). Among the overall group, average age was 12.6 years
(SD = 2.25), 51% was female, 49% Black, 40% Latinx, and
11% both Black and Latinx. AYALPHIV and AYAPHEU
participants did not significantly differ on any of these
demographic characteristics at enrollment (Table 1). Partici-
pants were followed up through FU7 at which point the
sample consisted of 206 adolescents and young adults (128
PHIV), and the average age was 24.6 years (SD = 2.60).
In the overall group, 76 of the 339 enrolled participants
(22%) reported a suicide attempt over the entire follow-up
period, and no instances of death by suicide were identified.
The prevalence of attempted suicide was significantly higher
among AYALPHIV compared with AYAPHEU (27% vs
16%, x2= 5.53, df = 1, P = 0.019).
In the overall group, the final model that predicted
suicide attempt over the course of follow-up through back-
ward stepwise logistic regression included HIV status, age,
family self-concept score, social self-concept score, CDI
score, and any DISC behavior disorder—all measured at
enrollment (Table 2). Notably, AYALPHIV had 2.21 times
the odds of making at least one suicide attempt over the
course of the longitudinal study compared with AYAPHEU
(95% CI: [1.18, 4.12], P = 0.013). The following measures at
enrollment were additionally associated with increased odds
of attempted suicide: older age, better social self-concept,
higher CDI score, and any DISC behavior disorder. Compar-
atively, better family self-concept seemed to be a protective
factor against attempted suicide.
When the sample was restricted to AYALPHIV, the
final model selected through backward stepwise logistic
regression included 2 of the same variables found in the
full-sample model: CDI score and any DISC behavior
disorder (Table 3). These variables were once again
TABLE 1. Description of CASAH Cohort by HIV Status
Total
(N = 339)
AYALPHIV*
(N = 206)
AYAPHEU*
(N = 133)
N (%)† N (%)† N (%)†
Attempted suicide 76 (22%) 55 (27%) 21 (16)
Male 167 (49%) 102 (50%) 65 (49%)
Female 172 (51%) 104 (51%) 68 (51%)
Identifies as straight/
heterosexual
227 (72%) 130 (69%) 97 (77%)
Race/ethnicity
Latinx 134 (40%) 73 (35%) 61 (46%)
Black/African
American
167 (49%) 105 (51%) 62 (47%)
Latinx and Black/
African American
36 (11%) 26 (13%) 10 (8%)
Mean (SD) Mean (SD) Mean (SD)
Age 12.58 (2.25) 12.70 (2.16) 12.38 (2.37)
City stress 0.66 (0.52) 0.62 (0.48) 0.73 (0.57)
Life events 1.31 (1.82) 1.34 (1.92) 1.27 (1.67)
Religiosity 2.76 (0.70) 2.75 (0.65) 2.79 (0.76)
Social problem-solving 2.36 (0.44) 2.34 (0.42) 2.39 (0.46)
Personal self-concept 4.00 (0.58) 3.96 (0.56) 4.06 (0.60)
Family self-concept 4.22 (0.62) 4.20 (0.61) 4.24 (0.63)
Social self-concept 3.98 (0.74) 3.99 (0.70) 3.98 (0.80)
Academic self-concept 3.84 (0.62) 3.77 (0.58) 3.93 (0.67)
Depression (CDI) 6.46 (5.66) 6.64 (5.90) 6.20 (5.29)
HIV stigma NA 1.77 (0.41) NA
N (%) N (%) N (%)
Missed medication in the past month NA 98 (57%) NA
DISC anxiety disorder 106 (31%) 63 (31%) 43 (32%)
DISC mood disorder 10 (3%) 7 (3%) 3 (2%)
DISC behavior disorder 23 (7%) 13 (6%) 10 (8%)
*AYALPHIV and AYAPHEU were compared on all table variables with 2
statistically significant differences: AYALPHIV had higher rates of suicide attempt
(Χ2 = 5.53 (1), P = 0.019) and lower academic self-concept (t = 2.28 (321), P = 0.023)
than AYAPHEU.
†Ns may not sum to total because of missing data. Percentages are of those with
nonmissing data. Percentages may not sum to 100 because of rounding.
HIV-Exposed But Uninfected Counterparts
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- 5. associated with significantly higher odds of attempted suicide.
In addition, religiosity was an important factor in the
AYALPHIV-specific model, with those with higher religios-
ity having significantly lower odds of attempted suicide.
When the sample was restricted to AYAPHEU, the
final model selected through backward stepwise logistic
regression included only the CDI score (Table 4). For every
one-point increase in CDI score, there was an 11% increase in
the odds of attempted suicide [OR = 1.11, 95% CI: (1.03 to
1.21), P = 0.011]. These results were similar to those in the
overall group [OR = 1.07, 95% CI: (1.01 to 1.14), P = 0.018]
and those in the AYALPHIV subsample [OR = 1.15, 95% CI:
(1.06 to 1.25), P = 0.001], situating early-life depressive
symptoms as a consistent risk factor of attempting suicide.
DISCUSSION
Reducing suicide among AYA remains a significant
challenge, and the findings in this study identify AYALPHIV
as a high-risk subgroup.9 Depressive symptoms (measured by
the CDI) in early adolescence were a predictor of attempted
suicide across all groups over time (total sample and
AYALPHIV and AYALPHEU subgroups). Among AYAL-
PHIV, higher religiosity seemed protective, whereas in the
overall group and among AYALPHIV, having a DISC
behavior disorder was associated with increased odds of
attempted suicide. These findings show the importance of
depressive symptoms in early adolescence for identifying
suicide risk and suggest the need for the development of
targeted early preventive interventions to address suicidality
among youth affected by HIV.
AYALPHIV had more than twice the odds of making a
suicide attempt when compared with AYAPHEU. Yet few
evidence-based interventions exist to address general AYAL-
PHIV mental health, and no interventions, to our knowledge,
specifically address suicidality among young people affected
by HIV.64,65 Our findings suggest an urgent need to tailor
suicide prevention interventions to the unique context and
challenges of early adulthood for AYALPHIV.66–69 Potential
interventions could consider approaches to support AYAL-
PHIV as they transition to adulthood.
It is well established that early-life depression is
associated with suicide.23–25 This analysis extends the field
by demonstrating that in early adolescence, symptoms of
depression, as measured by the CDI, were predictive of
attempted suicide over time whether or not AYA met
diagnostic criteria for a mood disorder, including major
depression, as measured by the DISC. This nuance suggests
that if researchers and practitioners restrict themselves to only
considering a diagnosis of major depressive disorder, they
may miss some young people who have significant symptoms
of depression, but do not yet meet diagnostic criteria and are
at risk of attempting suicide. Major depression and other
mood disorders often do not emerge until older adolescence
and young adulthood.70–72 Thus, understanding early symp-
toms may be important for prevention efforts. Furthermore,
given the brevity of the CDI tool, using the CDI (or other
symptom screens) may be feasible and actionable in many
low-resource contexts in the United States and elsewhere.
Mental health disorders, in particular depressive illness
and anxiety, have been consistently identified as risk factors
of suicidality among people living with HIV21,29–31 and HIV-
negative populations.23–28 Yet, to our knowledge, only one
previous study has examined correlates of suicidality among
AYALPHIV and youth affected by HIV.21 For the overall
group and for AYALPHIV, we found any DISC diagnosis of
behavior disorder at enrollment was highly predictive of
attempted suicide over time. Thus, our long-term follow-up
that examines attempted suicide into young adulthood adds to
the literature and highlights the importance of screening for
and addressing mental health among adolescents affected
by HIV.
In addition, we identified how psychosocial factors
such as self-concept affected the odds of attempting suicide
for adolescents affected by HIV. We approached self-concept
as a multifaceted construct and measured academic, personal,
family, and social domains separately.60 Our findings suggest
the importance of differentiating between different domains
of self-concept. In the overall group, having a higher family
self-concept was protective against suicidality. This finding is
consistent with international and US studies that suggest
TABLE 2. Backward Stepwise Logistic Regression Predicting
Attempted Suicide With Enrollment Demographic and
Psychosocial Variables Among Total CASAH Cohort (N = 309*)
Predictor OR (95% CI) P
HIV status 2.21 (1.18 to 4.12) 0.013
Age 1.18 (1.03 to 1.35) 0.018
Family self-concept 0.45 (0.25 to 0.81) 0.008
Social self-concept 1.75 (1.10 to 2.81) 0.019
Depression (CDI) 1.07 (1.01 to 1.14) 0.018
DISC behavior disorder 3.18 (1.22 to 8.29) 0.018
*Regression includes participants with no missing data.
TABLE 3. Backward Stepwise Logistic Regression Predicting
Attempted Suicide With Enrollment Demographic and
Psychosocial Variables Among AYALPHIV (N = 110*)
Predictor OR (95% CI) P
Religiosity 0.37 (0.17 to 0.78) 0.009
Depression 1.15 (1.06 to 1.25) 0.001
DISC behavior disorder 14.76 (1.37 to 158.90) 0.026
*Regression includes participants with no missing data.
TABLE 4. Backward Stepwise Logistic Regression Predicting
Attempted Suicide With Enrollment Demographic and
Psychosocial Variables Among AYAPHEU (N = 126*)
Predictor OR (95% CI) P
Depression (CDI) 1.11 (1.03 to 1.21) 0.011
*Regression includes participants with no missing data.
Kreniske et al J Acquir Immune Defic Syndr Volume 88, Number 4, December 1, 2021
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- 6. family structure and processes influence suicidality among
adults living with HIV29,73 and among adolescents who were
not affected by HIV.28,50,51,74 However, for the overall group,
a higher social self-concept (a measure largely focused on
peer relationships) was associated with increased odds of
suicidality, and this was consistent with one previous study
that identified interpersonal orientation as a predictor of
multiple suicide attempts among Black adolescents.75 This
finding warrants further investigation that would allow for an
in-depth examination of the potentially complex link between
higher social self-concept and suicidality among this
vulnerable group.
Of note, for AYALPHIV, we found higher religiosity
was associated with reduced odds of attempted suicide.
Previous studies examining the impact of religiosity on
suicidality offer mixed results. In the United States, a
longitudinal study of adolescents found lower religiosity
was protective against suicidal ideation almost one year
later.76 Other US studies have found no association between
religiosity and attempted suicide.77 In this study, we used one
measure of religiosity. However, religiosity is complex, and
more comprehensive work is needed to explore associations
between this construct and suicidality among AYALPHIV.
Many of the participants in this study, particularly
AYALPHIV, may have had access to mental health services
before, during, and after these FU visits. It is possible that rates
of attempted suicide would be even higher without such
services. In addition, the absence of an HIV-unexposed cohort
in this study limits our ability to fully discern the impact of HIV
on the health outcomes of HIV-affected AYA. Furthermore,
these findings may not be broadly generalizable to participants
not engaged in any kind of care system or people living with
HIV outside the US or even NYC. However, NYC is an
epicenter of the US epidemic, and demographics from CASAH
participants are similar to national studies of youth affected by
HIV, with AYALPHIV and AYAPHEU largely from inner-city,
low-income, ethnic minority families.78–80 Moreover, our results
align with previous studies in sub-Saharan Africa that suggest
the importance of mental health in understanding suicidality
among youth affected by HIV.21,49
The use of standardized and validated measures, including
the DISC, to assess mental health and attempted suicide was the
strength of this study.52,81,82 In addition, our multidimensional
measure of self-concept enabled us to examine how different
domains of self-concept functioned as protective and risk factors.
Furthermore, the longitudinal design of this study was a strength
and allowed for the examination of protective and risk factors of
attempted suicide among youth affected by HIV. Yet a limitation
was that we used a single survey round in early adolescence to
measure psychological profiles. Although the current research
offers a preliminary understanding of long-term protective and
risk factors of attempted suicide among youth affected by HIV,
future work should examine how these factors may change or
remain constant over time.
CONCLUSIONS
Suicide is a leading cause of death among young people
in the United States,1 and history of attempted suicide is a
strong predictor of eventual death by suicide.4–6 Our analyses
demonstrate that similar to other young people living with
chronic diseases,7 AYALPHIV are at increased risk of
attempted suicide. For AYALPHIV, early-life depressive
symptoms and having a behavior disorder were risk factors
of attempted suicide, whereas a positive family self-concept
and higher religiosity were protective. Similarly, among
AYAPHEU, early-life depressive symptoms were a risk
factor of attempted suicide. Our work presents an important
first step toward understanding the distal predictors of
attempted suicide among young people affected by HIV.
Further research, perhaps using mixed-methods, is needed to
examine these complex risk and protective factors.
REFERENCES
1. National Center for Injury Prevention and Control. 10 Leading Causes of Death
by Age Group, United States. Centers for Disease Control and Prevention.
Available at: https://www.cdc.gov/injury/wisqars/LeadingCauses_images.html.
Accessed August 2, 2021.
2. Burstein B, Agostino H, Greenfield B. Suicidal attempts and ideation
among children and adolescents in US emergency departments,
2007-2015. JAMA Pediatr. 2019;173:598.
3. Mishara BL, Stijelja S. Trends in US suicide deaths, 1999 to 2017, in the
context of suicide prevention legislation. JAMA Pediatr. 2020;174:
499–500.
4. Shaffer D, Gould MS, Fisher P, et al. Psychiatric diagnosis in child and
adolescent suicide. Arch Gen Psychiatry. 1996;53:339–348.
5. Borges G, Nock MK, Abad JMH, et al. Twelve-month prevalence of and
risk factors for suicide attempts in the world health organization world
mental health surveys. J Clin Psychiatry. 2010;71:1617–1628.
6. Glenn CR, Nock MK. Improving the short-term prediction of suicidal
behavior. Am J Prev Med. 2014;47:S176–S180.
7. Barnes AJ, Eisenberg ME, Resnick MD. Suicide and self-injury among
children and youth with chronic health conditions. Pediatrics. 2010;125:
889–895.
8. UNAIDS DATA. UNAIDS Joint United Nations Programme on HIV/
AIDS 20 Avenue Appia 1211 Geneva 27 Switzerland; 2019.
9. Kreniske P, Mellins CA, Dolezal C, et al. Sounding the alarm: perinatally
HIV-infected youth more likely to attempt suicide than their uninfected
cohort peers. J Adolesc Health. 2019;65:702–705.
10. Kalichman SC, Heckman T, Kochman A, et al. Depression and thoughts
of suicide among middle-aged and older persons living with HIV-AIDS.
PS. 2000;51:903–907.
11. Rundell JR, Kyle KM, Brown GR, et al. Risk factors for suicide attempts
in a human immunodeficiency virus screening program. Psychosomatics.
1992;33:24–27.
12. Ruffieux Y, Lemsalu L, Aebi-Popp K, et al. Mortality from suicide
among people living with HIV and the general Swiss population:
1988-2017. J Int AIDS Soc. 2019;22:e25339.
13. Croxford S, Kitching A, Desai S, et al. Mortality and causes of death in
people diagnosed with HIV in the era of highly active antiretroviral
therapy compared with the general population: an analysis of a national
observational cohort. Lancet Public Health. 2017;2:e35–e46.
14. Pelton M, Ciarletta M, Wisnousky H, et al. Rates and risk factors for
suicidal ideation, suicide attempts and suicide deaths in persons with
HIV: a systematic review and meta-analysis. Gen Psych. 2021;34:
e100247.
15. Dowshen N, D’Angelo L. Health care transition for youth living with
HIV/AIDS. Pediatrics. 2011;128:762–771.
16. Cluver LD, Gardner F, Operario D. Effects of stigma on the mental
health of adolescents orphaned by AIDS. J Adolesc Health. 2008;42:
410–417.
17. Menon A, Glazebrook C, Campain N, et al. Mental health and disclosure
of HIV status in Zambian adolescents with HIV infection: implications
for peer-support programs. J Acquired Immune Deficiency Syndromes.
2007;46:349–354.
18. Vreeman RC, McCoy BM, Lee S. Mental health challenges among
adolescents living with HIV. J Int AIDS Soc. 2017;20:21497.
HIV-Exposed But Uninfected Counterparts
J Acquir Immune Defic Syndr Volume 88, Number 4, December 1, 2021
Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved. www.jaids.com | 353
Copyright © 2021 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Downloaded
from
http://journals.lww.com/jaids
by
BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1A
WnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78=
on
03/05/2024
- 7. 19. Betancourt T, Scorza P, Kanyanganzi F, et al. HIV and child mental
health: a case-control study in Rwanda. Pediatrics. 2014;134:e464–472.
20. Mellins CA, Malee KM. Understanding the mental health of youth living
with perinatal HIV infection: lessons learned and current challenges. J Int
AIDS Soc. 2013;16:18593.
21. Ng LC, Kirk CM, Kanyanganzi F, et al. Risk and protective factors for
suicidal ideation and behaviour in Rwandan children. Br J Psychiatry.
2015;207:262–268.
22. Copelyn J, Thompson LC, Le Prevost M, et al. Self-harm in young
people with perinatal HIV and HIV negative young people in England:
cross sectional analysis. BMC Public Health. 2019;19:1165.
23. McLoughlin AB, Gould MS, Malone KM. Global trends in teenage
suicide: 2003–2014. QJM. 2015;108:765–780.
24. Feng CX, Waldner C, Cushon J, et al. Suicidal ideation in a community-
based sample of elementary school children: a multilevel and spatial
analysis. Can J Public Health. 2016;107:e100–e105.
25. May AM, Klonsky ED, Klein DN. Predicting future suicide attempts
among depressed suicide ideators: a 10-year longitudinal study. J
Psychiatr Res. 2012;46:946–952.
26. Melhem NM, Porta G, Oquendo MA, et al. Severity and variability of
depression symptoms predicting suicide attempt in high-risk individuals.
JAMA Psychiatry. 2019;76:603–613.
27. Geoffroy MC, Orri M, Girard A, et al. Trajectories of suicide attempts
from early adolescence to emerging adulthood: prospective 11-year
follow-up of a Canadian cohort. Psychol Med. 2020;15:1–11.
28. Dugas E, Low NCP, Rodriguez D, et al. Early predictors of suicidal
ideation in young adults. Can J Psychiatry. 2012;57:429–436.
29. Lu HF, Sheng WH, Liao SC, et al. The changes and the predictors of suicide
ideation and suicide attempt among HIV-positive patients at 6–12 months
post diagnosis: a longitudinal study. J Adv Nurs. 2019;75:573–584.
30. Carrico AW, Johnson MO, Morin SF, et al. Correlates of suicidal
ideation among HIV-positive persons. AIDS. 2007;21:1199–1203.
31. Egbe CO, Dakum PS, Ekong E, et al. Depression, suicidality, and alcohol
use disorder among people living with HIV/AIDS in Nigeria. BMC
Public Health. 2017;17:542.
32. Kim MH, Mazenga AC, Dev A, et al. Prevalence of depression and
validation of the beck depression inventory-II and the children’s
depression inventory-short amongst HIV-positive adolescents in Malawi.
J Int AIDS Soc. 2014;17:18965.
33. Dow DE, Turner EL, Shayo AM, et al. Evaluating mental health
difficulties and associated outcomes among HIV-positive adolescents
in Tanzania. AIDS Care. 2016;28:825–833.
34. Goldston DB, Molock SD, Whitbeck LB, et al. Cultural considerations in
adolescent suicide prevention and psychosocial treatment. Am Psychol.
2008;63:14–31.
35. McMahon EM, Keeley H, Cannon M, et al. The iceberg of suicide and
self-harm in Irish adolescents: a population-based study. Soc Psychiatry
Psychiatr Epidemiol. 2014;49:1929–1935.
36. Canetto SS, Sakinofsky I. The gender paradox in suicide. Suicide Life
Threat Behav. 2010;28:1–23.
37. Haas AP, Eliason M, Mays VM, et al. Suicide and suicide risk in lesbian,
gay, bisexual, and transgender populations: review and recommenda-
tions. J Homosex. 2011;58:10–51.
38. Assari S, Moghani Lankarani M, Caldwell CH. Discrimination increases
suicidal ideation in Black adolescents regardless of ethnicity and gender.
Behav Sci (Basel). 2017;7:75.
39. Oh H, Stickley A, Koyanagi A, et al. Discrimination and suicidality
among racial and ethnic minorities in the United States. J Affect Disord.
2019;245:517–523.
40. Polanco-Roman L, Anglin DM, Miranda R, et al. Racial/ethnic
discrimination and suicidal ideation in emerging adults: the role of
traumatic stress and depressive symptoms varies by gender not race/
ethnicity. J Youth Adolesc. 2019;48:2023–2037.
41. Lindsey MA, Sheftall AH, Xiao Y, et al. Trends of suicidal behaviors
among high school students in the United States: 1991–2017. Pediatrics.
2019;144:e20191187.
42. Durkheim É. Suicide. Routledge Kegan Paul Ltd: Paris, France; 1897.
43. Cha CB, Franz PJ, Guzmán EM, et al. Annual Research Review: suicide
among youth–epidemiology, (potential) etiology, and treatment. J Child
Psychol Psychiatry. 2018;59:460–482.
44. Franklin JC, Ribeiro JD, Fox KR, et al. Risk factors for suicidal thoughts
and behaviors: a meta-analysis of 50 years of research. Psychol Bull.
2017;143:187–232.
45. Ewart CK. Social action theory for a public health psychology. Am
Psychol. 1991;46:931–946.
46. Bridge JA, Goldstein TR, Brent DA. Adolescent suicide and suicidal
behavior. J Child Psychol Psychiatry. 2006;47:372–394.
47. Nrugham L, Larsson B, Sund AM. Predictors of suicidal acts across
adolescence: influences of familial, peer and individual factors. J Affect
Disord. 2008;109:35–45.
48. Prinstein MJ, Nock MK, Simon V, et al. Longitudinal trajectories and
predictors of adolescent suicidal ideation and attempts following
inpatient hospitalization. J Consult Clin Psychol. 2008;76:92–103.
49. Buckley J, Otwombe K, Joyce C, et al. Mental health of adolescents in
the era of antiretroviral therapy: is there a difference between HIV-
infected and uninfected youth in South Africa? J Adolesc Health. 2020;
67:76–83.
50. Sourander A, Klomek AB, Niemelä S, et al. Childhood predictors of
completed and severe suicide attempts: findings from the Finnish 1981
birth cohort study. Arch Gen Psychiatry. 2009;66:398–406.
51. Tuisku V, Kiviruusu O, Pelkonen M, et al. Depressed adolescents as
young adults - predictors of suicide attempt and non-suicidal self-injury
during an 8-year follow-up. J Affect Disord. 2014;152-154:313–319.
52. Shaffer D, Fisher P, Lucas CP, et al. NIMH Diagnostic Interview
Schedule for Children Version IV (NIMH DISC-IV): description,
differences from previous versions, and reliability of some common
diagnoses. J Am Acad Child Adolesc Psychiatry. 2000;39:28–38.
53. Shaffer D, Fisher P, Dulcan MK, et al. The NIMH diagnostic interview
schedule for children version 2.3 (DISC-2.3): description, acceptability,
prevalence rates, and performance in the MECA study. J Am Acad Child
Adolesc Psychiatry. 1996;35:865–877.
54. Kovacs M. Children’s Depression Inventory: Manual. New York, NY:
Multi-Health Systems North Tonawanda; 1992.
55. Mellins C, Havens J, Kang E. Child Psychiatry Service for Children and
Families Affected by the HIV Epidemic. IX International AIDS
Conference 1993: Berlin, Germany. Abstract PO-B35-2343, 1993.
56. Sarason IG, Johnson JH, Siegel JM. Assessing the impact of life changes:
development of the Life Experiences Survey. J consulting Clin Psychol.
1978;46:932.
57. Felitti VJ, Anda RF, Nordenberg D, et al. Relationship of childhood
abuse and household dysfunction to many of the leading causes of death
in adults: the adverse childhood experiences (ACE) study. Am J Prev
Med. 1998;14:245–258.
58. Ewart CK, Suchday S. Discovering how urban poverty and violence
affect health: development and validation of a Neighborhood Stress
Index. Health Psychol. 2002;21:254.
59. Holland JC, Kash KM, Passik S, et al. A brief spiritual beliefs inventory
for use in quality of life research in life-threatening illness. Psycho-
Oncology: J Psychol Soc Behav Dimensions Cancer. 1998;7:460–469.
60. Fitts WH, Roid GH. Tennessee Self Concept Scale. Counselor Record-
ings and Tests Nashville, TN; 1964.
61. Frauenknecht M, Black DR. Social Problem-Solving Inventory for
Adolescents (SPSI-A): development and preliminary psychometric
evaluation. J Personal Assess. 1995;64:522–539.
62. Chesney MA, Ickovics JR, Chambers DB, et al. Self-reported adherence
to antiretroviral medications among participants in HIV clinical trials: the
AACTG adherence instruments. Patient care committee adherence
working group of the outcomes committee of the adult AIDS clinical
trials group (AACTG). AIDS Care. 2000;12:255–266.
63. Fife BL, Wright ER. The dimensionality of stigma: a comparison of its
impact on the self of persons with HIV/AIDS and cancer. J Health Soc
Behav. 2000;41:50–67.
64. Bhana A, Abas MA, Kelly J, et al. Mental health interventions for
adolescents living with HIV or affected by HIV in low- and middle-
income countries: systematic review. BJPsych Open. 2020;6:e104. doi:
10.1192/bjo.2020.67.
65. Bhana A, Kreniske P, Pather A, et al. Interventions to address the mental
health of adolescents and young adults living with or affected by HIV:
State of the evidence. J Int AIDS Soc. 2021;24:e25713.
66. Arnett JJ. Emerging adulthood. A theory of development from the late
teens through the twenties. Am Psychol. 2000;55:469–480.
Kreniske et al J Acquir Immune Defic Syndr Volume 88, Number 4, December 1, 2021
354 | www.jaids.com Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved.
Copyright © 2021 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Downloaded
from
http://journals.lww.com/jaids
by
BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1A
WnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78=
on
03/05/2024
- 8. 67. Ferro MA, Gorter JW, Boyle MH. Trajectories of depressive symptoms
during the transition to young adulthood: the role of chronic illness. J
Affective Disord. 2015;174:594–601.
68. Leadbeater B, Thompson K, Gruppuso V. Co-occurring trajectories of
symptoms of anxiety, depression, and oppositional defiance from
adolescence to young adulthood. J Clin Child Adolesc Psychol. 2012;
41:719–730.
69. Hanghøj S, Boisen KA. Self-reported barriers to medication adherence
among chronically ill adolescents: a systematic review. J Adolesc Health.
2014;54:121–138.
70. Jane Costello E, Erkanli A, Angold A. Is there an epidemic of child or
adolescent depression?. J Child Psychol Psychiatry. 2006;47:1263–1271.
71. Kessler RC, Amminger GP, Aguilar-Gaxiola S, et al. Age of onset of
mental disorders: a review of recent literature. Curr Opin Psychiatry.
2007;20:359–364.
72. Kessler RC, Berglund P, Demler O, et al. Lifetime prevalence and age-
of-onset distributions of DSM-IV disorders in the national comorbidity
survey replication. Arch Gen Psychiatry. 2005;62:593–602.
73. Musisi S, Kinyanda E. Emotional and behavioural disorders in HIV
seropositive adolescents in urban Uganda. East Afr Med J. 2009;86:
16–24.
74. Matlin SL, Molock SD, Tebes JK. Suicidality and depression among
african American adolescents: the role of family and peer support and
community connectedness. Am J Orthopsychiatry. 2011;81:108–117.
75. Merchant C, Kramer A, Joe S, et al. Predictors of multiple suicide
attempts among suicidal Black adolescents. Suicide Life Threat Behav.
2009;39:115–124.
76. Nkansah-Amankra S, Diedhiou A, Agbanu SK, et al. A longitudinal
evaluation of religiosity and psychosocial determinants of suicidal
behaviors among a population-based sample in the United States. J
Affective Disord. 2012;139:40–51.
77. Ammerman BA, Serang S, Jacobucci R, et al. Exploratory analysis of
mediators of the relationship between childhood maltreatment and
suicidal behavior. J Adolescence. 2018;69:103–112.
78. Abrams EJ, Mellins CA, Bucek A, et al. Behavioral health and adult
milestones in young adults with perinatal HIV infection or exposure.
Pediatrics. 2018;142:e20180938.
79. Hall HI, Song R, Rhodes P, et al. Estimation of HIV incidence in the
United States. JAMA. 2008;300:520–529.
80. Moore RD. Epidemiology of HIV infection in the United States:
implications for linkage to care. Clin Infect Dis. 2011;52(Suppl 2):
S208–S213.
81. Asarnow J, McArthur D, Hughes J, et al. Suicide attempt risk in youths:
utility of the harkavy–asnis suicide scale for monitoring risk levels.
Suicide Life Threat Behav. 2012;42:684–698.
82. Goldston DB. Assessment of Suicidal Behaviors and Risk in Children
and Adolescents. National Institute of Mental Health (NIMH); 2000.
Available at: http://www.sprc.org/resources-programs/assessment-suicidal-
behaviors-risk-children-adolescents. Accessed August 2, 2021.
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