Comparison of Targeted and Routine Adolescent HIV Screening in a Pediatric Emergency Department

Abstract

Objectives:

The aims of the study were (1) to compare targeted and routine HIV screening in a pediatric emergency department (PED) and (2) to compare provider documented HIV risk assessment with adolescent perception of HIV risk assessment conducted during the PED visit.

Methods:

This prospective study ran concurrent to a PED routine HIV screening pilot. Adolescents could be tested for HIV by the PED provider per usual care (targeted testing); if not tested, they were approached for the routine screening pilot. A subset of adolescents completed a questionnaire on HIV risk. χ² analysis compared adolescents with targeted testing and routine screening. HIV-tested patients were asked if HIV risk was assessed; κ analysis compared this with documentation in the provider note.

Results:

Over 4 months, 107 adolescents received targeted testing and 344 received routine screening. One 14-year-old patient tested positive by routine screening; this adolescent had 2 PED visits without targeted testing within 60 days. Compared with routine screening, adolescents with targeted testing were more likely female (82% vs 57%, P < 0.001), 16 years or older (71% vs 44%, P < 0.001), or had genitourinary/gynecologic concerns (48% vs 6%, P < 0.001). Adolescents with HIV risk factors were missed by targeted testing but received routine screening. Adolescents with documented HIV risk assessment were more likely to receive targeted testing. There was moderate agreement (κ = 0.61) between provider documentation and adolescent perception of HIV risk assessment.

Conclusions:

There are gaps in PED HIV risk assessment and testing, which may miss opportunities to diagnose adolescent HIV. Routine HIV screening addresses these gaps and expands adolescent HIV testing in the PED.

In response to the HIV epidemic in the United States, the Centers for Disease Control and Prevention (CDC) recommend routine universal opt-out HIV screening for individuals 13 years and older in all healthcare settings.¹ Since 2006, this recommendation has aimed to increase the proportion of individuals diagnosed with early stage HIV, when initiation of antiretroviral therapy is most effective at improving immunologic outcomes and decreasing disease transmission.^2–4 Routine HIV screening has been implemented broadly in adults and particularly effective in the emergency department (ED).^5–7 Routine HIV screening is uncommon in adolescents, who continue to have high rates of HIV.⁸ Adolescents are a uniquely vulnerable population with high-risk sexual behaviors, low HIV screening rates, and fragmented healthcare access.^9–12 It is estimated that nearly half of HIV-infected adolescents are unaware of their infection and live with unrecognized disease for an average of 3 years before diagnosis.^13,14

In the absence of routine HIV screening, the default norm is targeted testing, in which the provider tests a patient for HIV on the basis of perceived risk or concerning symptoms.^1,15 In adults, routine screening in the ED increases testing and diagnosis compared with targeted testing.^5,16 Routine screening may be similarly beneficial in pediatric EDs (PEDs). Adolescents frequently seek care in the ED, where sexual histories are inadequately documented and may be unreliable for identifying those at risk for HIV.^17,18 Few PEDs have implemented routine screening,^19–23 and there have been no comparisons of adolescent ED patients who are tested for HIV through targeted testing and routine screening.

We have previously described our experiences implementing a PED HIV screening pilot, in which a convenience sample of adolescents was approached for routine screening.²³ During the pilot, providers were encouraged to offer HIV testing if they would otherwise do so as part of standard care (targeted testing). Adolescents were offered participation in the pilot if they did not receive targeted testing by their provider. We concurrently evaluated provider assessment of adolescent HIV risk, to identify points for intervention in future improvement efforts. As part of the quality assessment of the pilot, we aimed (1) to compare the characteristics of adolescents tested for HIV in the PED through provider-led targeted testing and the routine screening pilot, (2) to describe provider documentation of HIV risk, and (3) to compare provider documented HIV risk assessment to adolescent perception of HIV risk assessment.

METHODS

This prospective study took place during a pilot of routine adolescent HIV screening in the Children’s Healthcare of Atlanta Hughes Spalding Hospital PED.²³ Georgia has the highest rate of HIV in the United States, with most new diagnoses occurring in the Atlanta region.²⁴ Children’s Healthcare of Atlanta has a high rate of pediatric HIV (0.7% seroprevalence with targeted and diagnostic testing), 41% of whom have stage 3 HIV (formerly AIDS) at the time of diagnosis.²⁵ Hughes Spalding Hospital, in downtown Atlanta, is a freestanding academic children’s hospital with approximately 60,000 annual visits to the PED. This study was given the determination of nonhuman subjects research by the Emory and Children’s Healthcare of Atlanta Institutional Review Boards.

HIV Testing Procedures

The protocol for the routine adolescent HIV screening pilot has been described previously.²³ Briefly, adolescents were eligible for inclusion in this analysis if they were 13 to 18 years old, English or Spanish speaking, had no developmental delays or impaired mental status, were not critically ill, were not already diagnosed with HIV, and if they presented to the PED at a time when a pilot investigator was present to offer routine screening (40–60 h/wk). The PED providers were encouraged to offer HIV testing if they would otherwise do so as part of their usual practice (“targeted testing”). Unless triaged to the fast-track section of the PED, adolescents were not approached for screening until after they had been assessed by a provider (resident, nurse practitioner, attending physician). Fast-track patients are anticipated to have PED visits of less than 90-minute duration and without laboratory testing; these patients could be approached at any time after rooming. Eligible adolescents were approached for HIV education and those who had not received targeted testing by their PED provider were offered participation in pilot (“routine screening”). Any parent or guardian who was present for the PED visit was permitted to remain in the room while the screening team member met with the adolescent. In accordance with state law, adolescents gave verbal consent for HIV testing. HIV tests were run on serum samples using a fourth-generation assay in a central hospital laboratory. Institutional guidelines were in place for responding to positive results, which were communicated to the patient by the attending physician for diagnosis disclosure and linkage to outpatient care. Adolescents who were discharged before a positive result was available were called back to the ED by the primary investigator (C.K.G.) for diagnosis disclosure and linkage to outpatient care.

Data Collection

Demographic variables, including age, sex, race, ethnicity, and PED visit chief complaint, were collected from the electronic health record on all eligible adolescents who were tested for HIV. Age was categorized as younger adolescent (13–15 years) or older adolescent (16–18 years). Chief complaint was categorized a priori as genitourinary or gynecologic concern (GU/GYN) if there was dysuria, genital discharge, vaginal bleeding, pelvic pain, or similar symptoms. The PED provider note was reviewed to determine whether there was any documentation of HIV risk factors (defined as sexual activity or intravenous [IV] drug use). For patients with a positive HIV test, the electronic record was reviewed for associated laboratory testing (including HIV test results, other sexually transmitted infection [STI] test results, and CD4 count) and medical history (including basic details of prior PED visits).

To describe HIV risk in our adolescent population and to identify points for intervention in future improvement efforts, we designed a tablet-based questionnaire (Appendix 1, http://links.lww.com/PEC/A994). After undergoing Institutional Review Board review before study onset, the questionnaire was additionally reviewed by hospital administrators, who gave approval for the questionnaire halfway through the pilot implementation period (August 23, 2019), limited to older adolescents (Fig. 1). Adolescents gave written informed assent on the tablet before progressing to any additional items; there were no identifying items and responses were kept confidential from the clinical team. Questionnaire responses were linked with HIV screening results. The questionnaire, which was available in English and Spanish, included basic demographics (age, sex identity), sexual history, history of IV drug use, history of prior PED visits, history of STI testing and treatment, and prior HIVeducation. If present, the parent or guardian was permitted to remain in the room while the questionnaire was completed.

FIGURE 1.

Adolescent eligibility and participation in targeted HIV testing and the routine screening pilot.¹ These adolescents could receive targeted testing at provider discretion but are not included in the sample or analyses.² Exclusion criteria include: triage acuity level 1 (1), known HIV diagnosis (1), developmental delay and/or impairedmental status (70), and ineligible per provider (67).³ Reasons not approached include: discharged before able to be approached (123), repeat visits (68), and other (59).⁴ HIV testing of adolescents completing questionnaires: targeted testing (19), routine screening pilot (35), and declined testing (46).

To determine whether adolescents were aware when their PED provider sought to assess HIV risk, all eligible HIV-tested adolescents were asked, “Did your doctor or a member of your care team talk to you about HIV or sex during your emergency room visit today.” This question was asked verbally to all adolescents after the initial PED provider evaluation and was also incorporated into the questionnaire. If the parent or guardian had been present while meeting with the screening team, they remained in the room while this question was asked.

Statistical Analysis

Descriptive statistics, including means, standard deviations, counts, and proportions, were calculated for all variables of interest. Agreement statistics (Cohen κ) were used to compare the PED providers’ documentation of HIV risk assessment with the adolescents’ perceptions of HIV risk assessment during the visit. Given the limited number of written questionnaire responses to the question regarding HIV risk assessment, only the adolescents’ verbal responses were included in the agreement analysis. These were stratified by the presence or absence of a parent or guardian when the question was asked.

χ² and Fisher exact tests were used to compare demographic differences between the adolescents who received targeted HIV testing and the adolescents who received routine screening. Statistical significance was set at a P value of 0.05 or less. Statistical analysis was done using SAS 9.4 (Cary, NC) and R (R Core Team, 2020).

RESULTS

Over the 4-month period, there were 2954 adolescent PED visits. Of the 1168 (39%) eligible for participation (Fig. 1), 107 (9%) received targeted testing and 806 (69%) were approached for routine screening, of whom 344 (43%) participated. There was one positive test in a 14-year-old adolescent who received routine screening on the second of 2 PED visits during this period. Sexual history was not documented and targeted testing was not offered at either visit. This adolescent had a T-cell CD4 count greater than 500 (stage 1 HIV) and was connected to outpatient care within 1 week, started on antiretroviral therapy, and achieved an undetectable viral load. We have previously reported on the characteristics of the 462 adolescents who declined routine screening: there were no significant differences between adolescents who declined versus participated in routine screening by sex, ethnicity, race, reason for ED visit, or presence of parent, although adolescents who declined screening were more likely to be younger adolescents.²³

Table 1 shows the characteristics of adolescents receiving targeted testing and routine screening. Adolescents with targeted testing were more likely to be older (71% vs 44%, P < 0.001), female (82% vs 57%, P < 0.001), and to have presented for a GU/GYN concern (48% vs 6%, P < 0.001) than those receiving routine screening. Adolescents who received targeted testing were more likely to report an HIV risk assessment was performed by their PED provider (63% vs 18%, P < 0.001).

TABLE 1.

Demographics of Adolescents Receiving HIV Testing in the Pediatric Emergency Department

	Targeted Testing (n = 107)*	Routine Screening (n = 344)*	P
Age, n (%)			<0.001
13–15 y	28/98 (28.6)	193/344 (56.1)
16–18 y	70/98 (71.4)	151/344 (43.9)
Sex, female, n (%)	80/98 (81.6)	193/341 (56.6)	<0.001
Race, n (%)			0.21
White	7/98 (7.1)	13/342 (3.8)
Black or African American	90/98 (91.8)	327/342 (95.9)
Asian	1/98 (1)	0
American Indian and Alaska Native	0	1/342 (0.3)
Native Hawaiian/other Pacific Islander	0	1/342 (0.3)
Ethnicity, Hispanic or Latino, n (%)	5/95 (5.2)	12/344 (3.5)	0.38
Chief complaint, GU/GYN, n (%)	47/98 (48)	19/344 (5.5)	<0.001
Adolescent perception of HIV risk assessment, n (%)			<0.001
No HIV risk assessment by provider	19/51 (37.3)	226/277 (81.6)
HIV risk assessment by provider	32/51 (62.7)	51/277 (18.4)

^*Individual sample size varies because of missing data.

HIV risk was documented for 154 adolescents who received HIV testing (35% of 436 with available data). Adolescents with a documented HIV risk assessment were more likely to be older (67% vs 40%, P < 0.001), female (82% vs 51%, P < 0.001), to have presented for a GU/GYN concern (40% vs 1%, P < 0.001), and to receive targeted testing (57% vs 2%, P < 0.001) than those adolescents who did not have a documented HIV risk assessment (Table 2). There was moderate agreement between adolescent perception of an HIV risk assessment performed by their PED provider and documentation of HIV risk in the PED provider note (κ = 0.61; Table 3).

TABLE 2.

Demographics of Adolescents With and Without Provider-Documented HIV Risk Assessment

	HIV Risk Documented (n = 154)*	No HIV Risk Documented (n = 282)*	P
Age, n (%)			<0.001
13–15 y	50/152 (32.9)	168/281 (59.8)
16–18 y	102/152 (67.1)	113/281 (40.2)
Sex, female, n (%)	125/152 (82.2)	142/278 (51.1)	<0.001
Race, n (%)			0.32
White	8/151 (5.3)	12/280 (4.3)
Black or African American	141/151 (93.3)	267/280 (95.3)
Asian	1/151 (0.7)	0
American Indian and Alaska Native	0	1/280 (0.4)
Native Hawaiian/other Pacific Islander	1/151 (0.7)	0
Ethnicity, Hispanic or Latino, n (%)	8/150 (5.3)	9/281 (3.2)	0.28
Chief complaint, GU/GYN, n (%)	60/151 (39.7)	4/281 (1.4)	<0.001
HIV testing type, n (%)			<0.001
Targeted testing	88/154 (57.1)	5/282 (1.8)
Routine screening	66/154 (42.9)	277/282 (98.2)
Adolescent perception of HIV risk assessment, n (%)
No HIV risk assessment by provider	34/98 (34.7)	211/228 (92.5)	<0.001
HIV risk assessment by provider	64/98 (65.3)	17/228 (7.5)

^*Individual sample size varies because of missing data.

TABLE 3.

Agreement Between Providers’ Documentation and Adolescents’ Perception of HIV Risk Assessment

Subset	Adolescent Perception of HIV Risk Assessment	HIV Risk Documented (n = 98)	HIV Risk Not Documented (n = 228)	κ (95% CI)
All	No assessment	34 (34.7%)	211 (92.5%)	0.61 (0.41–0.74)
	Yes assessment	64 (65.3%)	17 (7.5%)
Parent present	No assessment	24 (40.0%)	159 (95.8%)	0.61 (0.49–0.73)
	Yes assessment	36 (60.0%)	7 (4.2%)
Parent absent	No assessment	10 (26.3%)	52 (83.9%)	0.58 (0.41–0.74)
	Yes assessment	28 (73.7%)	10 (16.1%)

CI indicates confidence interval.

Sixty-eight older adolescents received HIV testing and were eligible to complete the questionnaire (mean age, 16.7 years; 71% female; 40% targeted testing). Table 4 shows the characteristics of the 54 HIV-tested older adolescent respondents (79% response rate). There was no significant difference in age, sex, or parent presence between HIV-tested respondents and nonrespondents. Three adolescents (6%) reported a history of IV drug use. One male adolescent who received routine screening when presenting with nonspecific infectious symptoms disclosed on the questionnaire a history of oral and anal sex without condoms with 3 lifetime male sexual partners; he did not have a documented sexual history and was not offered targeted testing. Supplemental Table 1, http://links.lww.com/PEC/A995, includes the questionnaire responses of 46 adolescents who declined testing; compared with HIV tested adolescents, adolescents who completed the survey and declined HIV testing were less likely to be sexually active (37% vs 67%, P < 0.05) and more likely to report consistent condom use (22% vs 59%, P < 0.05).

TABLE 4.

Questionnaire Responses—HIV Risk Factors Reported by Adolescents Receiving HIV Screening

Adolescents Receiving HIV Screening	Targeted Testing (n = 19)	Universal Screening (n = 35)
Mean (SD) age, y*	16.7 (0.7)	16.7 (0.6)
Sex identity, n (%)
Male	3/19 (16)	10/35 (29)
Female	16/19 (84)	24/35 (69)
Male to female	0	0
Female to male	0	1/35 (2)†
IV drug use, yes, n (%)	1/19 (6)	2/35 (6)
Sexually active ever, yes, n (%)	18/19 (95)‡	18/35 (51)‡
No prior HIV education, n (%)	1 (5)	3 (9)
Prior HIV testing, n (%)
Yes, less than 6 mo ago	7 (36)	4 (11)
Yes, within 6–12 mo	0	3 (9)
Yes, more than 1 y ago	2 (11)	3 (9)
No	8 (42)	22 (62)
I don’t know	2 (11)	3 (9)
Sexually Active Adolescents Receiving HIV Screening§	Sexually Active, Targeted Testing (n = 18)	Sexually Active, Universal Screening (n = 18)
Sex of sexual partners of female adolescents, n (%)
Male	11/15 (73)	10/13 (77)
Female	0	1/13 (8)
Both	2/15 (13)	0
Sex of sexual partners of male adolescents, n (%)
Male	0	1/5 (20)
Female	3/3 (100)	4/5 (80)
Both	0	0
No. partners, n (%)
1	7/18 (39)	5/18 (28)
2–5	8/18 (44)	11/18 (61)
>5	3/18 (17)	1/18 (6)
Uses condoms always, n (%)	2/18 (11)	6/18 (35)
Prior STI testing, n (%)
Yes, have had positive test	2 (11)	3 (17)
Yes, never had positive test	10 (55)	4 (22)
Yes, don’t know results	1 (6)	2 (11)
No	2 (11)	7 (39)
I don’t know	3 (17)	2 (11)

^*Survey only offered to adolescents 16 to 18 years old.

^†Individual was never sexually active and was not included in below analyses of sexual activity by sex identity.

^‡P = 0.003.

^§Individual responses may not sum to total because of missing data.

DISCUSSION

There are clear gaps in HIV risk assessment and testing in adolescents receiving care in the PED. HIV risk assessments and standard of care targeted HIV testing were overwhelming directed toward older female adolescents who presented with GU/GYN symptoms. Targeted testing did identify a portion of adolescents at increased risk for HIV, yet many adolescents with HIV risk factors who were interested in HIV testing were missed by this strategy, including one adolescent who subsequently tested positive for HIV through routine screening. Implementation of CDC recommended routine HIV screening in adolescent PED patients may be an essential intervention to address gaps in HIV testing and slow progression of the HIV epidemic.

We found that providers who performed HIV testing focused primarily on a select subgroup of adolescents: older females with specific concerns potentially indicative of a STI. These adolescents certainly warrant consideration of testing for HIV. However, given the frequency of asymptomatic STIs, relying solely on symptoms of bacterial STIs is an ineffective way to identify adolescents at risk for HIV.²⁶ In addition, although young men continue to be disproportionately affected by HIV,⁸ they rarely received targeted testing. We have previously described a cohort of HIV-infected young adults whose diagnoses of HIV were potentially missed when they had presented to the PED in adolescence, the majority of whom were male.²⁷ In the current study, we also found that young adolescents were less likely to receive targeted testing. Although younger adolescents were more likely to decline routine screening,²³ and rates of HIV increase with adolescent age, it is important to note that the adolescent diagnosed with HIV in this pilot was a young 14-year-old patient who was missed by targeted testing twice during PED visits for seemingly minor concerns. With routine screening, this adolescent was diagnosed with early stage infection, when early antiretroviral initiation can mitigate the risk of secondary complications.^2,3 This highlights the importance of using the PED visit for HIV screening and diagnosis. Routine HIV testing reached a broader group of interested adolescents, with near equal representation by sex and age.

Among older adolescents, we found that many of those with risk factors for HIV, including those with multiple sexual partners, those with inconsistent condom use, and men who have sex with men, were missed by targeted testing. Consistent with previous research,¹⁷ adolescent sexual histories were uncommon in this PED, occurring for only one-third of adolescent visits and biased toward older, female adolescents with symptoms potentially suggestive of a STI. The PED providers are often managing multiple patients of varying levels of acuity and may be concerned about the time required to gather a sexual history on every adolescent patient. Routine screening can obviate this concern and further provides a degree of normalization appealing to adolescents that may reduce stigma and bias.

There have been efforts to develop clinical predictive tools that decrease the burden and cost of testing on individuals with no or low HIV risk. This strategy has been successful in adults when implemented into nursing intake²⁸ but has not been evaluated in adolescents and would require unique considerations to confidentiality. For adolescents, routine computer-assisted self-interviews have been used in the PED to collect confidential sexual histories and can increase STI testing.²⁹ Future research is needed to determine whether such tools can increase the efficacy of targeted HIV testing in the adolescent PED population and to explore the cost-effectiveness of various testing strategies.

The American Academy of Pediatrics promotes the role of the pediatrician in providing sexual health care and, along with the Society for Adolescent Health and Medicine, promotes adolescent confidentiality.^30,31 Furthermore, providing sexual healthcare in the PED has been identified as acceptable by adolescents, parents, providers, and PED leaders.^32–34 Despite these national standards, demonstrated acceptability, and prior IRB review, we faced administrative concerns that delayed the distribution of our questionnaire and prevented us from collecting HIV risk data in young adolescents. Concerns regarding adolescent sexual healthcare are unlikely to be a barrier unique to our institution. There continues to be a need to better understand and address such concerns, so as to best provide high-quality and equitable healthcare to the most marginalized adolescent populations.

We found that adolescent perception of the HIV risk assessment did not always align with provider documentation of a HIV risk. There are several possible explanations for this finding. First, it is possible that adolescents were not aware that providers had attempted to ask about sexual activity and HIV risk. A PED visit may be stressful or frightening and adolescents may be distracted during history taking, particularly if they do not recognize how the discussion impacts their PED presentation. Second, previous studies have demonstrated that adolescent disclosure of sexual activity may not be reliable.^18,35 Adolescents frequently seek care in the ED,¹² where they are unlikely to have existing trust relationships with providers. In this context, adolescents may be reluctant to disclose risk factors and/or remember the conversation. This may also be influenced by the provider’s comfort level in discussing sexual health with the adolescent. Finally, it is possible that adolescents did not want to disclose that they had discussed HIV risk, particularly if their parent/guardian was in the room when this was assessed. However, we found no differences in adolescent perception of an HIV risk assessment when stratified by parent presence. Furthermore, the HIV screening team performed HIV education and screening before asking adolescents whether their provider had performed an HIV risk assessment, so it may be unlikely that adolescents would then be reluctant to disclose that they had discussed these topics with their provider.

This study is subject to several limitations. First, we approached a convenience sample of adolescents based on availability of the HIV screening team, although our team focused on the times of day when adolescent PED visits were most common and were available for a variety of day and night shifts on both weekdays and weekends. Second, this study took place in a region with high HIV prevalence after multiple years of provider education and efforts to increase PED-based HIV testing. This single-center study is not intended to be generalizable. It is likely that more adolescents received targeted testing than in other centers that have not received such focused intervention. Adolescents were only eligible for routine screening if they did not first receive targeted testing. Providers in our PED were aware of the ongoing routine HIV screening pilot and were subject to the Hawthorne effect. However, we cannot predict in which direction this may have influenced provider behaviors, as some providers may have been more likely to test for HIV because of the constant reminder of the ongoing pilot, while others may have been less likely to test by assuming patients would be tested through the pilot. Finally, because of administrative concerns regarding adolescent sexual health topics, we were unable to assess HIV risk factors in our entire cohort. However, we had a high response rate despite low overall numbers of completed questionnaires.

The PED visit is an essential opportunity to address the epidemic of adolescent HIV. Despite CDC recommendations for universal screening in all adolescents, targeted testing and late diagnosis remain the norm. We found gaps of care in PED HIV risk assessment and testing, leading to missed opportunities to diagnose adolescent HIV. Routine HIV screening can address gaps of care and expand adolescent HIV testing in the PED.

Supplementary Material

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.pec-online.com).