Improved prevention of mother-to-child transmission of HIV (PMTCT) programs and the rollout of universal antiretroviral treatment have resulted in a significant decrease in the number of children living with HIV.1 Strengthened early infant diagnosis (EID) programs, the implementation of international and national guidance to address specific needs of children living with HIV, and improved formulations for pediatric antiretroviral therapy (ART) have improved access to and quality of pediatric HIV treatment. Despite these advances, however, in 2013, only 24% of the estimated 3.2 million children living with HIV were on ART.2 Half of these children would die before their second birthday without ART.3 Among children on ART, up to two-thirds were diagnosed late and began treatment with severe immunodeficiency.4
The Accelerating Children's HIV/AIDS Treatment Initiative (ACT) responded to these shortcomings in pediatric diagnosis and treatment. Implemented from 2014 to 2016 with funding from the US President's Emergency Plan for AIDS Relief (PEPFAR) and the Children's Investment Fund Foundation (CIFF), ACT was a $200 million initiative to accelerate the ART coverage of HIV-infected children and adolescents in sub-Saharan Africa. The third pillar of the ACT initiative focused on systematically improving HIV case identification among children through strengthening EID, index case finding (ICF), and provider-initiated testing and counseling (PITC) in priority pediatric services.5 With an intensified global emphasis on pediatric case finding, the proportion of children on ART globally increased to 43% in 2016.1 Despite this progress, novel, high-yield approaches to case finding are urgently needed to reach the 57% of HIV-infected children still not on ART.
Despite facing a higher risk of HIV infection, many children of HIV-infected adults have not been tested.6,7 Family testing is an ICF approach wherein patients enrolled in ART programs are screened for untested family members, and it may be an efficient strategy to increase the diagnosis of perinatally infected children (Table 1).
Case identification is a critical step in preventing morbidity and mortality from HIV infection. Traditionally, EID and PITC have been the cornerstone of case identification in children. Although these approaches successfully identify a substantial proportion of children living with HIV, gaps in case finding persist and HIV-infected children remain undiagnosed.
Gaps in Case Finding With EID
As most pediatric HIV cases are due to vertical transmission, EID programs play a critical role in identifying HIV-infected children before they become symptomatic. Although PMTCT has improved significantly over the past several years, allowing for increased enrollment of HIV-exposed infants into EID programs, gaps persist: lack of universal ART coverage of HIV-infected mothers, late incident infection among pregnant and breastfeeding women, and mother–infant pairs lost to follow-up that result in ongoing HIV transmission and missed opportunities for case finding.6–10 Once children age out of EID programs, opportunities for systematic HIV screening among healthy children are rare.
Gaps in Case Finding With PITC
PITC refers to HIV testing initiated by a health worker, typically at a health facility. This can take many forms, from routine opt-out testing for all patients to targeted testing of sick patients with symptoms suggestive of AIDS. PITC is a critical component of the larger care cascade, although significant shortcomings limit its utility for pediatric case finding. Health workers are reluctant to offer testing to children, especially if they are asymptomatic, due to misperception of risk or concerns regarding consent.8 Pilot studies of universal pediatric testing at venues such as immunization clinics have been promising but are resource-intensive and dramatically increase the burden on counselors.9 The relatively low HIV prevalence among children and the large number accessing immunization clinics may limit the feasibility and value of this approach in some settings.10
In addition, as children age, their utilization of primary health services where PITC can be delivered declines and orients instead around sick visits and inpatient admissions. As a result, most children identified through PITC are already acutely ill when diagnosed,11 and almost all missed earlier opportunities for diagnosis.8 Other barriers to optimized PITC include lack of child-friendly services and variable interpretation of PITC guidelines.12
ICF is a Potential Solution to Fill These Gaps
EID and PITC are critical approaches; however, alone they are insufficient in closing the pediatric HIV case finding gap. Less than half of HIV-infected children are on treatment, and of those who have initiated ART up to 63% in lower middle-income countries were already severely immunocompromised upon initiation.3,10
Even in optimized systems, children fall through the cracks. The likelihood of early diagnosis without supplemental case finding is low, and without treatment, presentation with symptomatic illness or advanced stage disease is more likely and risk of death increases. In one region of Harare, Zimbabwe—where PMTCT and EID outcomes are relatively strong—a community survey after several years of implementation of routine facility-based opt-out pediatric PITC found that over a third of HIV-infected children remained undiagnosed, and that PITC identified only 29% of previously undiagnosed children.13 Thus, reliance on facility-based PITC alone, even when well-implemented, may miss most children and identify only those who have already developed symptomatic disease. A realistic, systematic approach to pediatric case finding is therefore necessary, one that recognizes the inherent shortcomings of imperfect systems and deploys pragmatic, high-yield strategies in response.
ICF is a WHO-endorsed approach in which contacts of an HIV-infected individual (the “index” case) are offered HIV counseling and testing. For the children of HIV-infected adults, this approach is generally referred to as family testing.
Family testing is a type of ICF in which HIV testing is offered to sexual partners as well as other family members of an HIV-infected patient, including siblings and parents of HIV-infected children. In this approach, index cases can be adults or children. Family testing is a pragmatic, high-yield, and acceptable approach to close the diagnosis gap among children by identifying those missed by EID and PITC programs and to reach children living with HIV before they become ill.
The children of HIV-infected adults have a higher risk of infection,14 and up to 65% of undiagnosed children have a family member already enrolled in an ART program.8,11 Despite this concentration of risk, screening of active cohorts of ART clients for untested family members and notification for testing at baseline is poor—among children of HIV-infected mothers, often less than half (and as low as 10%) access testing services.7,15–17 These children can be screened, diagnosed, and treated earlier by systematically screening HIV-infected patients, and integrating systems for appropriate case finding and referral.
Family Testing is an Effective Method for Identifying Children Living With HIV
Family testing of children consistently demonstrates a higher yield of new diagnoses compared with other modalities because of its targeting of a high-risk population. In Kenya, yield of testing was 7.4%—higher than both the general population and what would be expected in EID with effective PMTCT—and most children were asymptomatic at the time of diagnosis with a median CD4 of 666.6 Serial reports from Kenyan districts that have implemented family testing indicate a declining yield over time (18% in 2009 to 5.4% in 2015), yet even the lowest yield is over 3-fold higher than pediatric PITC at the same facilities.18–20 In Malawi, more than two-thirds of index patients enrolled in ART were found to have an untested child, and of these, 4% tested positive, more than twice the estimated prevalence for this age group.21 Family testing of children also promotes uptake of HIV testing across the family unit.22
Family testing should be offered to any child with unknown HIV status whose parent or sibling is the index patient, regardless of the child's age. The limited disaggregation of results by age among studies of family testing makes interpretation of yield by age category difficult. In Uganda, uptake and yield were both higher in the 5 and under group compared with the 6–14 group; however, analysis of yield was not conducted according to age categories.23 The very limited data comparing testing yields for children who are and those who are not biologic offspring or siblings of the index patient suggest similar yields for the 2 groups,21,23 potentially due to the unique risks to which children living outside of the nuclear family are exposed. More evidence is needed before routine inclusion of children without direct biologic relationship to the index patient can be recommended as a routine component of index testing programs.
Barriers in Implementing Family Testing
Family testing requires active participation from providers and index patients, from the point of screening index patients for family members with unknown status, to linking newly identified HIV-infected child contacts to treatment (Fig. 1). Implementation studies have demonstrated highly variable rates of attrition across the ICF cascade. In Kenya, of 611 index patients with a child of unknown status, only 74 (12%) completed testing for their child. The reason for falling out of the cascade for 83% of index patients was declined participation.6 An earlier study in Kenya found that among children of ART patients identified during screening, only one-third accessed testing, and of those found positive, 36% initiated ART.19
Results from Malawi are more promising, with 94% of eligible index patients consenting to family testing. Index patients were offered a choice between home- and facility-based testing, with a majority (88%) opting for home-based testing. Among children found to be positive, 77% were enrolled into HIV care.21 This high rate of linkage may be a reflection of the study's implementation as part of a robust community health worker platform with a strong track record for pediatric diagnosis and linkage to care.24 Preliminary results from Cameroon also demonstrated excellent acceptability, with 100% of eligible adults consenting. Index patient preference for testing location differed, however, with 93% opting for facility-based testing—almost the opposite of that reported in Malawi.25
Reported rates of uptake of HIV testing of children are highly variable, ranging from 19% to 94%.6,18–23,25,26 Currently available evidence is limited in explaining this variability. It is plausible that testing location may affect uptake. In a randomized trial in Uganda including all household members, home-based testing was associated with a 10-fold higher rate of uptake compared with facility-based testing, an effect that was even greater in child contacts.23 Of note, the 2 studies with the highest acceptance rates (Malawi and Cameroon) offered clients a choice of testing location. Although the venue patients chose in these studies differed, the simple ability to choose may mark a patient-centered approach that improves testing uptake.
Future studies on barriers to testing specific to this approach are needed for programs to optimize uptake; however, lessons may be drawn from the existing literature describing general barriers to pediatric testing. These barriers fit into several thematic categories: individual, caregiver, health system, and policy/legal barriers. Barriers include attitudes and language exhibited by health care workers, index patients feeling unprepared to disclose own status to children/partner, avoidance of blame, guilt, and stigma, and fear of positive results (Table 2).28,29
Need for Systematic and Ongoing Family Testing
Embracing family testing as a routine, ongoing assessment of HIV status rather than a 1-time referral is critical to optimizing uptake and limiting attrition across the cascade. A systematic assessment of ART patients' family contacts and repeat referral as new contacts are identified is associated with high uptake.18,21 At each clinic visit, contacts of index clients who have tested negative should be evaluated for ongoing risk according to national HIV testing service (HTS) guidelines and be offered retesting as needed. Use of dedicated tools to map family members that include each individual's HIV status is critical to implementation and is associated with higher rates of index screening and family testing, along with linkage to care for newly diagnosed children.18,21,26,37
CURRENT POLICY GUIDELINES
Although further research will help optimize family testing programs, the available evidence suggests that family testing is an efficient, high-yield intervention that should be leveraged to close the gap in pediatric case finding. Despite recent global guidance (Table 3) emphasizing the importance of index testing, current country guidelines vary in the amount of detail they include regarding ICF strategies for children, as well as in policies around consent, which directly impact the uptake of ICF for children (Table 4).
Novel Approaches/Future Directions
Assisted partner notification is a well-established, effective, and safe approach to promote testing of HIV-exposed contacts and involves active participation of the health provider in disclosure and invitation of contacts for testing. Integration of family-linked testing for children into existing assisted partner notification programs for adults may be pragmatic and efficient for leveraging the existing notification platform to prioritize testing of another high-risk population—the children of index cases. The one study that has examined the feasibility of this approach demonstrated a low yield (2%), but almost 100% acceptance rate,48 warranting further investigation of this strategy. Self-testing is a promising approach to increase uptake of testing among contacts of index patients and may promote testing of children, especially with the use of less-invasive oral tests; however, no evidence describing this approach is available.
RECOMMENDATIONS, FUTURE RESEARCH
Gaps in traditional pediatric case finding approaches limit progress toward the 90-90-90 goals for children. Family testing is a high-yield and promising approach to diagnose children who fall through the gaps in traditional case finding programs and should be integrated into routine programming to ensure that children are not missed. We recommend that all countries define a policy for family testing in their national guidelines that includes, at a minimum, active screening of HIV-infected clients for family members with unknown HIV status and follow-up for testing, with linkage to care for newly identified HIV-infected persons. To facilitate implementation, guidelines should outline a minimum standard package of tools, standard operating procedures (SOPs), and guidance. The complexity of the intervention may vary by country and implementer, but systematic screening and referral for testing should be ensured.
A comprehensive family testing package may include the following components:
- Clear definition of an index patient as any HIV-infected person, including adults, adolescents, and children. All should be screened for untested contacts requiring referral for testing, including parents, children, siblings, sexual partners, and drug-injecting contacts.
- Clearly defined policies for assent, consent, and disclosure for children, with tools to train providers in these concepts, including child-friendly health services and ongoing monitoring to ensure correct implementation.
- Behavior change communication strategies to improve community understanding of HIV risk among children and the importance of family index testing and timely linkage to care for HIV-infected individuals.
- Toolkit (see Annex 1, Supplemental Digital Content, http://links.lww.com/QAI/B187):
- (1)Family testing screening form: A simple tool to facilitate active screening of index clients for untested contacts. A screening tool is best incorporated into existing ART clinic patient records, but in cases where this is not possible, it may be included as part of a discrete screening tool. Most effective if the contact information is located where it is easily reviewed at every index client visit. Includes the following information:
- (a) Index patient: name, locator information, # children, and # sexual partners
- (b) For each identified contact: HIV status, test dates, and ART status
- (c) Additional considerations:
- (i) Include location preference for testing (home vs facility)
- (ii) Include a preidentified appointment date for contacts to return for testing
- (2)Family testing register and monthly report: A register and monthly report to monitor performance along the family testing cascade from HIV testing to ART initiation for positives. Routine reporting should include a clearly defined family testing cascade. Countries may choose to use a specific index testing register or to incorporate the information into existing HTS registers, but should, at a minimum, track the following information:
- (a) Number of index patients
- (b) Number of contacts
- (c) Number of contacts with known vs unknown status
- (d) Number of contacts tested
- (e) Number of contacts diagnosed with HIV
- (f) Number of HIV+ contacts started on ART
- (3)Script to support disclosure to/invitation of contacts: A sample disclosure script empowering a patient to bring contacts for testing facilitates comprehensive, consistent delivery of counseling to index patients and may help improve contacts' return for testing.
- (4)SOP for family testing and linkage to care: An SOP outlining processes and tools assists program managers with streamlined implementation from screening through linkage of positives.
In some settings, delivery of a comprehensive family testing package may require stepwise implementation; however, countries should, at a minimum, aim to urgently implement a family testing model in which all HIV-infected patients are screened at least once to identify children of unknown status using a simple family screening tool maintained as part of the active ART client record.
Given the sensitive nature of HIV testing, family testing approaches should be implemented carefully and in close collaboration with civil society partners. The complex issues of confidentiality, stigma, and disclosure that arise from HIV testing for children must be considered, and this approach cannot succeed at scale unless it is implemented in a manner that supports families.
Future qualitative research to understand the widely variable uptake in testing for children described in implementation studies of ICF may inform policy and practice to address barriers affecting uptake of testing among child contacts. Further investigation of the utility of assisted partner notification strategies for identifying both perinatally and horizontally infected youth may result in additional strategies to complement existing case finding approaches.
Finally, family testing programs must not be implemented in isolation, but rather as a critical component of a comprehensive package of pediatric case finding approaches. Continued strengthening of existing EID and PITC programs must be undertaken to ensure that no children are left undiagnosed.
Despite improvements in EID and PITC in recent years, significant numbers of HIV-infected children are not accessing lifesaving ART. Broad implementation of strategies such as index family testing is urgently needed to diagnose these children and link them to care. By screening known HIV-infected persons for untested family members, family testing offers a pragmatic, high-yield, and efficient approach for resource-constrained health systems to reach these children and connect them to care before they become sick. To optimize uptake, programs should routinely and repeatedly screen all HIV-infected patients and refer any untested family contacts for testing. By supporting this approach with clear and concrete policy guidance, engaging civil society to ensure appropriate community support and empowering program managers to implement family testing models tailored to their country settings, and national ART programs have an opportunity to close the gaps in pediatric case finding and ensure that children do not fall further behind in reaching the 90-90-90 targets.
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