Pediatric Tuberculosis Infection Care Facilitators and Barriers: A Qualitative Study Free

We conducted in-depth individual interviews and small group discussions (SGDs) with clinicians and individual interviews with caregivers to identify facilitators and barriers to the completion of the TB infection care cascade. Study reporting follows the COnsolidated criteria for REporting Qualitative research guidelines.²² This study was approved by the Boston Children’s Hospital Institutional Review Board.

We recruited clinicians for individual interviews by contacting attending pediatricians working in Boston clinics by direct e-mail. Potential participants were identified from webpages of area clinics and purposefully sampled from (1) federally qualified health centers (FQHC), (2) non-FQHC clinics located in communities with large immigrant populations, (3) non-FQHC clinics operating in locations with low numbers of immigrants, (4) TB or infectious diseases clinics, and (5) subspecialty clinics treating children and adolescents receiving immunosuppressive medications (eg, patients with rheumatologic conditions). We identified potential participants for SGDs by contacting clinicians at Boston-area primary care and TB or infectious disease clinics.

We identified English- and Spanish-speaking patients <18 years old at the time of TB infection diagnosis within a large pediatric hospital system in Boston. Caregivers were identified by using administrative data ascertained from a previous cohort study in which the authors evaluated the completion of the pediatric TB infection care cascade.⁷ We invited the primary caregivers of eligible patients by mail and telephone. Participants were purposefully sampled to represent caregivers of patients who both had and had not completed the TB infection care cascade, as determined in the previous study.⁷ 

For clinician interviews and SGDs, we developed semi-structured interview guides on the basis of a review of the TB infection care cascade literature.²³ With the questions and probes, we sought to examine perceived facilitators and barriers to engagement in TB infection care, individual and clinic-wide strategies to engage patients in care, and stories about patients who engaged and disengaged in care. To discuss and brainstorm solutions to gaps in care engagement in SGDs, we developed vignettes of mock patients who disengaged from TB infection care at different points in the care cascade (Supplemental Information). SGD participants were asked to describe their approach to reengaging these mock patients. All clinician participants completed questionnaires about comfort with TB infection care recommendations.

For caregiver interviews, we developed a semi-structured interview guide informed by our previous care cascade investigation⁷ and the Framework for Access to Healthcare.²⁴ A certified service translated the guide into Spanish. Interviews were conducted in English or Spanish (facilitated by trained medical interpreters), per caregiver preference. After the interview, participants completed a questionnaire about knowledge, attitudes, and beliefs surrounding TB infection.²⁵ 

Because interviews and SGDs took place during the coronavirus disease 2019 pandemic (2021–2022), they were all conducted virtually using video conferencing (Zoom Video Communications, Inc). Two investigators trained in qualitative methods (YA, JIC) conducted the interviews and SGDs. Video and audio files were recorded, and audio files were transcribed verbatim (and translated, if needed) by a professional transcription service (Datagain). Interview guides are included in the Supplemental Information. All participants provided written informed consent electronically and received a $50 gift card after study completion. Interviews lasted ∼30 minutes, and SGDs lasted ∼1 hour.

We used applied thematic analysis to analyze qualitative data. First, interview transcripts were reviewed as interviews were conducted to identify key emergent concepts. After the completion of all interviews, 2 researchers (JIC, YA/MT) rereviewed transcripts in a first immersion and crystallization process, during which key ideas were elicited and data saturation was determined. Relevant and recurrent content was organized into codebooks. We developed separate codebooks for individual clinician interviews, SGDs, and caregiver interviews. The codebooks included prespecified deductive codes to characterize facilitators and barriers to cascade completion, as well as inductive codes representing emergent and unanticipated concepts. The codebooks were imported into an electronic software package (NVivo). Two researchers (JIC, YA/MT) independently coded all transcripts. To ensure interrater reliability, we compared coded transcripts side-by-side in multiple comparison meetings.

After coding completion, codes and coded text were reviewed in a second immersion and crystallization step to identify themes pertinent to TB infection care retention. The themes were mapped onto social levels drawing from socioecological theory²⁶ and integrated into a comprehensive model for care engagement. To ensure credibility, the process of identifying themes was discussed at multiple meetings with study team members involved in coding, as well as in 2 triangulation meetings with team members not involved in data acquisition. We used summary and descriptive statistics to analyze questionnaire responses.

A total of 25 and 30 clinicians were invited to participate in individual interviews and SGDs, of whom 14 and 10 participated, respectively. Three SGDs enrolled primary care clinicians, and 1 SGD enrolled clinicians working in a TB clinic. A total of 62 caregivers were invited to participate in individual interviews, of whom 19 enrolled. Participant characteristics are detailed in Tables 1 and 2.

Clinicians were generally comfortable with TB infection recommendations. Primary care and immunocompromised host clinicians reported a relatively high volume of TB infection testing per year but infrequently diagnosed TB infections (Table 1). Caregivers expressed a range of beliefs and attitudes toward TB infection.

We identified themes relating to community and health system and family and patient factors that drove or inhibited engagement in TB infection care. The interaction of these key themes with care engagement steps is shown in Fig 1, which represents a conceptual model for pediatric TB infection care engagement across socioecological levels and is supported by themes and quotations described below.

Clinicians noted that targeted testing protocols and questionnaires enabled the systematic evaluation of high-risk groups, including new immigrants and patients receiving immunomodulatory therapy (Table 3). The use of preprogrammed pathways and order sets in the electronic medical record (eg, “new immigrant order set”) was helpful in remembering to order TB testing. Clinicians also identified gaps in these protocols, including a lack of clarity regarding country-specific TB risk, uncertainty about TB risk factors besides travel, and the type of testing to administer based on age. One gap involved a lack of protocols to enable the screening of individuals not directly receiving a clinician’s care (eg, parents encountered in a nursery).

Clinicians noted challenges for patients returning for tuberculin skin test (TST) reads. Clinicians often preferred obtaining interferon-γ release assays (IGRAs), particularly if other bloodwork was also needed. However, some physicians explained that IGRAs can be technically challenging in the setting of fear of needles and difficult blood draws, particularly for small children. Additionally, clinicians noted that interpretation of TB test results could be challenging and that TB diagnostics are “a complicated field.”

Clinicians used multiple education techniques to relay the TB infection diagnosis and its attendant risks, including discussing the risks of TB infection before testing, using chest radiographs as a visual aid, and explaining that TB infection could be a public health risk if it progresses to TB disease. Despite an acknowledged imperative to communicate TB risks to patients, clinicians noted that time constraints in clinics could limit their ability to have important but often lengthy conversations.

Clinicians described a range of clinical contact they maintained throughout the diagnostic and treatment steps of the care cascade. Frequent clinical contact could sustain patients’ care engagement; however, caregivers and some clinicians commented that frequent clinic visits became a barrier to remaining in care.

Limited clinic hours were a major barrier to care and created disruptions for children receiving treatment. For instance, limited clinic hours meant that patients would need to miss school, which was problematic when frequent in-person check-ins were required for children on therapy. Although the frequency of check-ins varied, monthly visits were most common.

Inconveniently located clinics also hindered access to TB infection care, particularly when care for rural-dwelling patients was provided at centralized (typically urban) TB clinics. Colocation of clinic services could overcome place-related barriers to engaging in care.

Inconvenient and expensive transportation impeded routine follow-up. Clinicians described a variety of available programs (eg, public medical transportation vouchers) designed to overcome these barriers.

Communication and cooperation, or lack thereof, between multiple clinicians caring for patients at risk for and with TB infection affected engagement. In particular, the interface between primary care and TB or infectious diseases clinics was both a barrier and facilitator to sustained care. Some clinicians cited disruptions and logistical challenges when referring to a TB specialist. Others commented on the importance of TB specialist input, both as a resource regarding treatment regimens and to build trust with families and patients.

Interpreters and multilingual providers were critical members of team-based management for communicating key medical information and engendering trust, although communication barriers could persist even with interpreters.

Insurance-related barriers primarily arose with TB infection testing. Clinicians’ concerns about the costs and cost-effectiveness of IGRAs motivated the ongoing use of TSTs. Others noted that private insurance could be a disadvantage for obtaining testing because it would not always cover IGRAs.

The availability of free medication at TB clinic pharmacies was seen as a key advantage of these clinics and a driver of referral.

Clinicians noted that the ability to monitor prescription refills (facilitated by electronic health record tools) was helpful for tracking medication adherence. However, they recognized that even these approaches to adherence monitoring provided a partial view of sustained adherence.

Shorter treatment regimens were widely acknowledged to improve adherence. However, comfort with these regimens varied. One primary care clinician commented that increasing use of shorter, rifamycin-based regimens led to more referrals to TB clinics for the initiation and management of treatment, primarily stemming from a lack of familiarity with initiating shorter regimens. Additionally, a unique challenge regarding treatment regimen selection referenced by TB clinicians included concerns regarding nitrosamine contamination of rifamycin drugs in the United States. Concerns about exposing children to nitrosamines led TB clinicians to engage in in-depth risk–benefit counseling in light of official cautions regarding rifamycin use.

Regimen selection often hinged on patients’ underlying conditions and perceived ability to tolerate regimens. Regimens were not always convenient for children with medical complexity. One caregiver described challenges with administering pill or tablet formulations to her son, who required medication administration via a gastrostomy tube.

Clinicians referred to the challenge of motivating patients and caregivers to adhere to medication for an asymptomatic infection. Motivational interviewing and emphasizing the future risk of TB were ways to overcome this barrier.

Caregivers described the fear of side effects as a limitation of medication adherence. Clinicians noted that frequent communication and the immediate ability to address emerging side effects helped address concerns.

A diagnosis of TB infection could be stigmatizing, and caregiver concerns about stigma were often amplified by beliefs about infectiousness, with the difference between TB “infection” and “disease” not always apparent to caregivers, relatives, other close contacts, or school officials (Table 4). TB stigma inhibited some patients’ and families’ willingness to accept a TB infection diagnosis or discuss TB infection with clinicians.

Caregivers drew on multiple information sources that informed their knowledge and beliefs about TB infection and treatment, including personal experiences with TB, family members and friends, and health care professionals. Preconceptions about the safety of long-term medication regimens were a common barrier to therapy initiation.

Testing was a major source of distrust in TB infection management. For families reluctant to accept a TB infection diagnosis, the perceived unreliability of TB tests and their results (caregivers were particularly skeptical of TSTs in the setting of Bacille Calmette-Guerin [BCG] vaccination) engendered feelings of distrust that impeded both perceived risk and willingness to initially engage in additional diagnostics or treatment. Some caregivers specifically asked for a “confirmatory” blood test if a TST result was positive. However, if both a TST and IGRA were performed, discordant TST and IGRA results further contributed to the perceived unreliability of testing.

A cultural connection between clinicians and patients and families was seen as critical to engaging patients in the initial steps of care. Clinicians noted that speaking the same language as families created cultural connection and trust.

Clinicians commented that caregiver oversight was critical for adherence. Conversely, a lack of caregiver oversight was particularly problematic for some newly immigrated adolescent patients, who often navigated an unfamiliar health care system with little support.

Clinicians noted broad challenges in engaging adolescents in TB infection care. As adolescents’ autonomy emerged, they were often charged with attending clinic appointments on their own or were solely responsible for remembering to take their medication. These responsibilities were uniquely challenging for adolescents who lacked insight into TB infection.

Caregivers and clinicians noted medication adherence could be challenging for children who rejected medications because of taste or side effects. Patients and families would often “get tired” of taking medications, particularly when unconvinced of their utility.

Caregivers discussed techniques they used to remember medication administration, including phone alarms, family calendars to coordinate between caregivers, and the use of routines. External “nudges” propelled caregivers and patients through each TB infection care step. For instance, caregivers were motivated to have their children tested for TB when required by daycare facilities or schools. Additionally, clinicians perceived that a treatment completion letter motivated adherence.

Clinicians and caregivers noted that if families were struggling with housing, transportation, or immigration status, or if caregivers were working multiple jobs or faced their own medical conditions, supporting daily medication adherence became difficult. TB infection care was not a priority for some families; for example, one caregiver described balancing TB infection care for one child while managing another child’s complex chronic conditions.

The inability to get to appointments or pick up medications could impair engagement in care and impose financial strains. Caregivers cited easing transportation barriers as a reason to transfer TB infection care from central TB clinics to primary care clinics.

In the setting of competing demands, a strong social support system aided TB infection care completion. For example, social support enabled clinic attendance in the setting of competing time and parenting demands. A lack of support was burdensome for families that had recently immigrated. Clinics were often able to provide material support for these families.

TB infection affected children living in diverse family and household environments, including multigenerational or split households. Communication and coordination between family members facilitated care, whereas a lack of communication and coordination could lead to nonadherence and disengagement.

Figure 2 summarizes key barriers and solutions derived from or explicitly recommended by participants.

Informed by our qualitative results, we developed a consolidated framework integrating facilitators and barriers across the pediatric TB infection care cascade (Fig 1). Many of the identified themes (eg, the role of trust, the intersection of immigration and adolescence, and the balance of families’ competing demands) have not been widely described in previous qualitative or quantitative studies of pediatric TB infection.

Our findings reveal the psychological effects of the diagnosis and treatment of TB infection in children. Multiple themes capture both the stress for patients and caregivers and techniques to mitigate this stress. Key sources of stress included the energy, time, and resource demands involved in sustaining care, which often intersected with the material and emotional challenges faced by immigrants from countries with high TB prevalence who needed to quickly learn to navigate a new health care system.²⁷ Our findings also emphasize the challenges that adolescents face when engaging in TB infection care. Adolescents have been identified as requiring unique TB care engagement strategies,²⁸ and our findings suggest that the intersection of new immigration and adolescence can produce distinct challenges (eg, “early adulting”) leading to loss from care.

Cultural norms, stigma, and misinformation affected patients’ and caregivers’ willingness and motivation to engage in care. Stigma and unwillingness to disclose TB infection to others may have prevented caregivers from accessing social support from friends and relatives. Diverse and often negative beliefs about TB have been documented in other populations,^29,30 and clinicians in our study described spending significant time and effort elucidating and discussing patients’ and caregivers’ preconceptions about TB infection with variable success. Ongoing attention to culturally specific TB-related counseling may improve trust between caregivers and clinicians, particularly at the intersection of TB, immigration, and social drivers of health.³¹ 

Clinicians and caregivers identified facilitators and barriers to care access that have been addressed in recent changes in US pediatric TB infection care. First, recent US recommendations have deemphasized the use of TST in favor of IGRAs, including for young children.³² Clinicians in our study noted IGRAs also posed challenges, particularly when the result was indeterminate, laboratory resources were unavailable, and young children were resistant to phlebotomy. Our findings illustrate how the technical limitations of TB infection tests^33,34 translate into distrust between caregivers and clinicians and substantial time and resource strain on families requiring multiple visits for testing (either for TST reads or repeat IGRAs after indeterminate results). Second, our results illustrate how recommendations to use short-course regimens prompted increased referrals to TB clinics despite policy efforts to shift TB infection care to primary care. Others have raised concerns that knowledge gaps surrounding rifamycin-based regimens impede TB infection care delivery in primary care.^21,35 Our findings provide empirical evidence for this concern and highlight a specific opportunity for education or other innovative methods for managing these patients in primary care (eg, with telehealth consultation). Third, our study coincided with concerns about nitrosamine contamination in rifamycin drugs in the United States. Clinicians described needing to revamp adherence monitoring strategies and risk and benefit counseling in response to published warnings regarding rifamycin use.

Participants identified multiple solutions to common barriers to care engagement. At the clinic and health system level, solutions targeted streamlining clinical decision-making and decreasing cognitive load in busy clinical environments (eg, improving functionality, accessibility, and specificity of TB risk questionnaires). Improved documentation and care coordination pathways could also mitigate losses from the cascade that occur during clinical transfers. Suggested patient- and caregiver-level tools to improve care frequently related to adherence reminder and promotion strategies. Although mHealth and eHealth systems may fill some of the identified adherence gaps,³⁶ scaling these systems will require dedicated funding and implementation strategies.

Our study has limitations. First, findings may differ in other settings with different TB public health delivery strategies, availability of public insurance, and populations. Second, caregivers of children who did not complete the cascade were underrepresented in our study, and we may not have fully captured this population’s perspectives. Third, we conducted interviews with caregivers in English and Spanish because these were the predominant languages represented in our previous cohort study.⁷ However, we may have missed insights from cultural groups who were not included.

Our study offers a lens into the complex ecosystem of pediatric TB infection care engagement. Building from clinician and caregiver insights, we built a comprehensive model of pediatric TB infection care engagement anchored in socioecological theory and the TB infection care cascade. This model provides a logistical framework for addressing the complexity and challenges associated with pediatric TB infection care. It can also inform future targeted interventions to improve diagnosis and treatment completion in clinical practice.

We acknowledge the study participants for their time and enthusiasm.

FQHC

federally qualified health centers

IGRA

interferon-γ release assay

SGD

small group discussion

TB

tuberculosis

TST

tuberculin skin test